Skip to main content

Developmental Aspects of Sleep

  • Chapter
  • First Online:
Pediatric Sleep Medicine

Abstract

Sleep undergoes remarkable changes during early development in humans and the most studied experimental model rat. Albeit practical challenges, it is interesting to study the macro- and micro-architecture of EEG during critical stages of development to get an insight into the neuronal plasticity involved in network formation for the complex process of sleep-wakefulness. Various clues derived from experimental condition including sleep deprivation during pregnancy have aided in the understanding of distinct time-line defined development of sleep. Understanding of sleep-wakefulness during development can provide important clues about associated disorders in sleep architecture, sleep bouts and sleep fragmentation. Detection of sleep changes in neonates may be of great clinical significance and can be viewed as an early marker of psychobehavioural disorders that may appear later in life.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. McCarley RW. Neurobiology of REM and NREM sleep. Sleep Med. 2007;8:302–30.

    Article  PubMed  Google Scholar 

  2. Mackiewicz M, Naidoo N, Zimmerman JE, Pack AI. Molecular mechanisms of sleep and wakefulness. Ann N Y Acad Sci. 2008;1129:335–49.

    Article  PubMed  Google Scholar 

  3. Saper CB, Fuller PM, Pedersen NP, Lu J, Scammell TE. Sleep state switching. Neuron. 2010;68:1023–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW. Control of sleep and wakefulness. Physiol Rev. 2012;92:1087–187.

    Article  CAS  PubMed  Google Scholar 

  5. Wigren HK, Porkka-Heiskanen T. Novel concepts in sleep regulation. Acta Physiol. 2018;222:e13017.

    Article  CAS  Google Scholar 

  6. Roffwarg HP, Muzio JN, Dement WC. Ontogenetic development of the human sleep-dream cycle. Science. 1996;152:604–19.

    Article  Google Scholar 

  7. Jouvet-Mounier D, Astic L, Lacote D. Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol. 1970;2:216–39.

    Article  CAS  PubMed  Google Scholar 

  8. Menna-Barreto L, Benedito-Silva AA, Marques N, de Andrade MMM, Louzada F. Ultradian components of the sleep-wake cycle in babies. Chronobiol Int. 1993;10:103–8.

    Article  CAS  PubMed  Google Scholar 

  9. Karlsson KAE, Gall AJ, Mohns EJ, Seelke AMH, Blumberg MS. The neural substrates of infant sleep in rats. PLoS Biol. 2005;3:e14.

    Article  CAS  Google Scholar 

  10. Korotchikova I, Stevenson NJ, Livingstone V, Ryan CA, Boylan GB. Sleep-wake cycle of the healthy term newborn infant in the immediate postnatal period. Clin Neurophysiol. 2016;127:2095–101.

    Article  PubMed  Google Scholar 

  11. Aswathy BS, Kumar VM, Gulia KK. The effects of rapid eye movement sleep deprivation during late pregnancy on newborns’s sleep. J Sleep Res. 2018;27:197–205.

    Article  CAS  PubMed  Google Scholar 

  12. Aswathy BS, Kumar VM, Gulia KK. Immature sleep pattern in newborn rats when dams encountered sleep restriction during pregnancy. Int J Dev Neurosci. 2018;69:60–7.

    Article  CAS  PubMed  Google Scholar 

  13. Gramsbergen A, Schwartze P, Prechtl HF. The postnatal development of behavioral states in the rat. Dev Psychobiol. 1970;3:267–80.

    Article  CAS  PubMed  Google Scholar 

  14. Dreyfus-Brisac C. Ontogenesis of sleep in human prematures after 32 weeks of conceptional age. Dev Psychobiol. 1970;3:91–121.

    Article  CAS  PubMed  Google Scholar 

  15. Prechtl HF. The behavioural states of the newborn infant (a review). Brain Res. 1974;76:185–212.

    Article  CAS  PubMed  Google Scholar 

  16. Andre M, Lamblin MD, d’Allest AM, Curzi-Dascalova L, Moussali-Salefrangue F, Nguyen ST, Veccierini-Blineau MF, Wallois-Esquivel E, Plouin P. Electroencephalography in premature and full-term infants. Developmental features and glossary. Neurophysiol Clin. 2010;40:59–124.

    Article  CAS  PubMed  Google Scholar 

  17. Korte J, Wulff K, Oppe C, Siegmund R. Ultradian and circadian activity-rest rhythms of preterm neonates compared to full-term neonates using actigraphic monitoring. Chronobiol Int. 2001;18:697–708.

    Article  CAS  PubMed  Google Scholar 

  18. Curzi-Dascalova L, Figueroa JM, Eiselt M, Christova E, Virassamy A, d’Allest AM, Guimarâes H, Gaultier C, Dehan M. Sleep state organization in premature infants of less than 35 weeks’ gestational age. Pediatr Res. 1993;34:624–8.

    Article  CAS  PubMed  Google Scholar 

  19. Szeto HH, Hinman DJ. Prenatal development of sleep-wake patterns in sheep. Sleep. 1985;8:347–55.

    Article  CAS  PubMed  Google Scholar 

  20. Umans JG, Cox MJ, Hinman DJ, Dogramajian ME, Senger G, Szeto HH. The development of electrocortical activity in the fetal and neonatal guinea pig. Am J Obstet Gynecol. 1985;153:467–71.

    Article  CAS  PubMed  Google Scholar 

  21. Frank MG, Heller HC. Development of diurnal organization of EEG slow-wave activity and slow-wave sleep in the rat. Am J Phys. 1997;273:R472–8.

    CAS  Google Scholar 

  22. Adams SM, Jones DR, Esmail A, Mitchell EA. What affects the age of first sleeping through the night? J Paediatr Child Health. 2004;40:96–101.

    Article  CAS  PubMed  Google Scholar 

  23. Jaffa T, Scott S, Hendriks JH, Shapiro CM. ABC of sleep disorders. Sleep disorders in children. BMJ. 1993;306:640–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. de Weerd AW, van den Bossche RAS. The development of sleep during the first months of life. Sleep Med Rev. 2003;7:179–91.

    Article  PubMed  Google Scholar 

  25. Valatx JL. The ontogeny and physiology confirms the dual nature of sleep states. Arch Ital Biol. 2004;142:569–80.

    CAS  PubMed  Google Scholar 

  26. Blumberg MS, Seelke AMH, Lowen SB, Karlsson KÆ. Dynamics of sleep-wake cyclicity in developing rats. Proc Natl Acad Sci U S A. 2005;102:14860–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Karlsson KAE, Blumberg MS. The union of the state: myoclonic twitching is coupled with nuchal muscle atonia in infant rats. Behav Neurosci. 2002;116:912–7.

    Article  PubMed  Google Scholar 

  28. Losito E, Eisermann M, Vignolo P, Hovhannisyan S, Magny JF, Kaminska A. Benign neonatal sleep myoclonus evokes somatosensory responses. J Clin Neurophysiol. 2017;34:484–91.

    Article  PubMed  Google Scholar 

  29. Feng P. Neonates. In: Kushida CA, editor. Sleep deprivation: clinical issues, pharmacology, and sleep loss effects, Lung biology in health and dsease. New York: CRC Press; 2002. p. 121–42.

    Google Scholar 

  30. Garcia-Rill E, Buchanan R, McKeon K, Skinner RD, Wallace T. Smoking during pregnancy: postnatal effects on arousal and attentional brain systems. Neurotoxicology. 2007;28:915–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Richardson HL, Walker AM, Horne RSC. Maternal smoking impairs arousal patterns in sleeping infants. Sleep. 2009;32:515–21.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Mennella JA, Garcia-Gomez PL. Sleep disturbances after acute exposure to alcohol in mothers’ milk. Alcohol Fayettev. 2001;25:153–8.

    Article  CAS  Google Scholar 

  33. Hilakivi L. Effects of prenatal alcohol exposure on neonatal sleep-wake behaviour and adult alcohol consumption in rats. Acta Pharmacol Toxicol. 1986;59:36–42.

    Article  CAS  Google Scholar 

  34. Bard KA, Coles CD, Platzman KA, Lynch ME. The effects of prenatal drug exposure, term status, and caregiving on arousal and arousal modulation in 8-week-old infants. Dev Psychobiol. 2000;36:194–212.

    Article  CAS  PubMed  Google Scholar 

  35. Davidson JO, Quaedackers JS, George SA, Gunn AJ, Bennet L. Maternal dexamethasone and EEG hyperactivity in preterm fetal sheep. J Physiol. 2011;589:3823–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Gulia KK, Patel N, Radhakrishnan A, Kumar VM. Reduction in ultrasonic vocalizations in pups born to rapid eye movement sleep restricted mothers in rat model. PLoS One. 2014;9:e84948.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Gulia KK, Patel N, Kumar VM. Increased ultrasonic vocalizations and risk-taking in rat pups of sleep-deprived dams. Physiol Behav. 2015;139:59–66.

    Article  CAS  PubMed  Google Scholar 

  38. Gulia KK, Kumar VM. Ultrasonic vocalizations and behavior of rat pups born from sleep-deprived dams. In: Brudzynski SM, editor. Handbook of behavioral neuroscience series, Handbook of ultrasonic vocalizations-a window into the emotional bain publisher: Elsevier; 2018. p. 467–78.

    Google Scholar 

  39. Radhakrishnan A, Aswathy BS, Kumar VM, Gulia KK. Sleep deprivation during late pregnancy produces hyperactivity and increased risk-taking behavior in offspring. Brain Res. 2015;1596:88–98.

    Article  CAS  PubMed  Google Scholar 

  40. Olischar M, Klebermass K, Waldhoer T, Pollak A, Weninger M. Background patterns and sleep-wake cycles on amplitude-integrated electroencephalography in preterms younger than 30 weeks gestational age with peri−/intraventricular haemorrhage. Acta Paediatr Oslo Nor. 2007;96:1743–50.

    Article  Google Scholar 

  41. Ardura J, Andrés J, Aldana J, Revilla MA. Development of sleep-wakefulness rhythm in premature babies. Acta Paediatr Oslo Nor. 1995;84:484–9.

    Article  CAS  Google Scholar 

  42. Holditch-Davis D. The development of sleeping and waking states in high-risk preterm infants. Infant Behav Dev. 1990;13:513–31.

    Article  Google Scholar 

  43. Foreman SW, Thomas KA, Blackburn ST. Preterm infant state development. J Obstet Gynecol Neonatal Nurs. 2008;37:657–65.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Mrdalj J, Pallesen S, Milde AM, Jellestad FK, Murison R, Ursin R, Bjorvatn B, Grønli J. Early and later life stress Alter brain activity and sleep in rats. PLoS One. 2013;8:e69923.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Tiba PA, Tufik S, Suchecki D. Effects of maternal separation on baseline sleep and cold stress-induced sleep rebound in adult wistar rats. Sleep. 2004;27:1146–53.

    Article  PubMed  Google Scholar 

  46. Gunnar MR, Cheatham CL. Brain and behavior interface: stress and the developing brain. Infant Ment Health J. 2004;24:195–211.

    Article  Google Scholar 

  47. Pollmächer T, Mullington J, Lauer CJ. REM sleep disinhibition at sleep onset: a comparison between narcolepsy and depression. Biol Psychiatry. 1997;42:713–20.

    Article  PubMed  Google Scholar 

  48. Mamelak M. Narcolepsy and depression and the neurobiology of gammahydroxybutyrate. Prog Neurobiol. 2009;89:193–219.

    Article  CAS  PubMed  Google Scholar 

  49. Borbély AA. The S-deficiency hypothesis of depression and the two-process model of sleep regulation. Pharmacopsychiatry. 1987;20:23–9.

    Article  PubMed  Google Scholar 

  50. Mendelson WB, Sack DA, James SP, Martin JV, Wagner R, Garnett D, Milton J, Wehr TA. Frequency analysis of the sleep EEG in depression. Psychiatry Res. 1987;21:89–94.

    Article  CAS  PubMed  Google Scholar 

  51. Hoffmann R, Hendrickse W, Rush AJ, Armitage R. Slow-wave activity during non-REM sleep in men with schizophrenia and major depressive disorders. Psychiatry Res. 2000;95:215–25.

    Article  CAS  PubMed  Google Scholar 

  52. Cusmano DM, Mong JA. In utero exposure to valproic acid changes sleep in juvenile rats: a model for sleep disturbances in autism. Sleep. 2014;37:1489–99.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Rao U, McGinty DJ, Shinde A, McCracken JT, Poland RE. Prenatal stress is associated with depression-related electroencephalographic sleep changes in adult male rats: a preliminary report. Prog Neuro-Psychopharmacol Biol Psychiatry. 1999;23:929–39.

    Article  CAS  Google Scholar 

  54. Field T, Diego M, Hernandez-Reif M, Schanberg S, Kuhn C, Yando R, Bendell D. Pregnancy anxiety and comorbid depression and anger: effects on the fetus and neonate. Depress Anxiety. 2003;17:140–51.

    Article  PubMed  Google Scholar 

  55. Röschke J, Prentice-Cuntz T, Wagner P, Mann K, Frank C. Amplitude frequency characteristics of evoked potentials during sleep: an analysis of the brain's transfer properties in depression. Biol Psychiatry. 1966;40:736–43.

    Article  Google Scholar 

  56. Gall AJ, Joshi B, Best J, Florang VR, Doorn JA, Blumberg MS. Developmental emergence of power-law wake behavior depends upon the functional integrity of the locus coeruleus. Sleep. 2009;32:920–6.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Levitt MZ, Selman RL, Richmond JB. The psychosocial foundations of early adolescents’ high-risk behavior: implications for research and practice. J Res Adolesc. 1991;1:349–78.

    Article  Google Scholar 

  58. Weisman O, Magori-Cohen R, Louzoun Y, Eidelman AI, Feldman R. Sleep-wake transitions in premature neonates predict early development. Pediatrics. 2011;128:706–14.

    Article  PubMed  Google Scholar 

  59. Kintraia PI, Devdariani MG, Kokhiia MI, Mikadze SI. Diagnostic value of particularities of circadian rhythms of sleep-wake cycle in early ontogenesis. Georgian Med News. 2006:7–9.

    Google Scholar 

  60. Sivadas N, Radhakrishnan A, Aswathy BS, Kumar VM, Gulia KK. Dynamic changes in sleep pattern during post-partum in normal pregnancy in rat model. Behav Brain Res. 2017;320:264–74.

    Article  PubMed  Google Scholar 

  61. Nishina H, Honda K, Okai T, Kozuma S, Inoué S, Taketani Y. Characteristic changes in sleep patterns during pregnancy in rats. Neurosci Lett. 1966;203:5–8.

    Article  Google Scholar 

  62. Wilson DL, Barnes M, Ellett L, Permezel M, Jackson M, Crowe SF. Decreased sleep efficiency, increased wake after sleep onset and increased cortical arousals in late pregnancy. Aust N Z J Obstet Gynaecol. 2011;51:38–46.

    Article  PubMed  Google Scholar 

  63. Driver HS, Shapiro CM. A longitudinal study of sleep stages in young women during pregnancy and postpartum. Sleep. 1992;15:449–53.

    Article  CAS  PubMed  Google Scholar 

  64. Suchecki D, Tiba PA, Tufik S. Paradoxical sleep deprivation facilitates subsequent corticosterone response to a mild stressor in rats. Neurosci Lett. 2002;320:45–8.

    Article  CAS  PubMed  Google Scholar 

  65. Maccari S, Morley-Fletcher S. Effects of prenatal restraint stress on the hypothalamus–pituitary–adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology. 2007;32:S10–5.

    Article  CAS  PubMed  Google Scholar 

  66. Maccari S, Darnaudery M, Van Reeth O. Hormonal and behavioural abnormalities induced by stress in utero: an animal model for depression. Stress Amst Neth. 2001;4:169–81.

    CAS  Google Scholar 

  67. Wirz-Justice A, Kräuchi K, Brunner DP, Graw P, Haug HJ, Leonhardt G, Sarrafzadeh A, English J, Arendt J. Circadian rhythms and sleep regulation in seasonal affective disorder. Acta Neuropsychiatr. 1995;7:41–3.

    Article  CAS  PubMed  Google Scholar 

  68. Dugovic C, Maccari S, Weibel L, Turek FW, Van Reeth O. High corticosterone levels in prenatally stressed rats predict persistent paradoxical sleep alterations. J Neurosci. 1999;19:8656–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Mairesse J, Silletti V, Laloux C, Zuena AR, Giovine A, Consolazione M, van Camp G, Malagodi M, Gaetani S, Cianci S, Catalani A, Mennuni G, Mazzetta A, van Reeth O, Gabriel C, Mocaër E, Nicoletti F, Morley-Fletcher S, Maccari S. Chronic agomelatine treatment corrects the abnormalities in the circadian rhythm of motor activity and sleep/wake cycle induced by prenatal restraint stress in adult rats. Int J Neuropsychopharmacol. 2013;16:323–38.

    Article  CAS  PubMed  Google Scholar 

  70. Kimura M, Curzi ML, Romanowsi CPN. REM sleep alteration and depression. Arch Ital Biol. 2014;152:111–7.

    CAS  PubMed  Google Scholar 

  71. McGraw K, Hoffmann R, Harker C, Herman JH. The development of circadian rhythms in a human infant. Sleep. 1999;22:303–10.

    Article  CAS  PubMed  Google Scholar 

  72. Reiter RJ, Tan DX, Korkmaz A, Rosales-Corral SA. Melatonin and stable circadian rhythms optimize maternal, placental and fetal physiology. Hum Reprod Update. 2014;20:293–307.

    Article  CAS  PubMed  Google Scholar 

  73. Kennaway DJ, Stamp GE, Goble FC. Development of melatonin production in infants and the impact of prematurity. J Clin Endocrinol Metab. 1992;75:367–9.

    CAS  PubMed  Google Scholar 

  74. Ozdemir OM, Ergin H, Sahiner T. Electrophysiological assessment of the brain function in term SGA infants. Brain Res. 2009;1270:33–8.

    Article  PubMed  CAS  Google Scholar 

  75. Cohen E, Wong FY, Wallace EM, Mockler JC, Odoi A, Hollis S, Horne RSC, Yiallourou SR. EEG power spectrum maturation in preterm fetal growth restricted infants. Brain Res. 1678;2018:180–6.

    Google Scholar 

  76. Dube J, Lafortune M, Bedetti C, Bouchard M, Gagnon JF, Doyon J, Evans AC, Lina JM, Carrier J. Cortical thinning explains changes in sleep slow waves during adulthood. J Neurosci. 2015;35:7795–807.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Tekell JL, Hoffmann R, Hendrickse W, Greene RW, Rush AJ, Armitage R. High frequency EEG activity during sleep: characteristics in schizophrenia and depression. Clin EEG Neurosci. 2005;36:25–35.

    Article  PubMed  Google Scholar 

  78. Samson-Dollfus D, Nogues B, Menard JF, Bertoldi-Lefever I, Geffroy D. Delta, theta, alpha and beta power spectral of sleep electroencephalogram in infants aged two to eleven months. Sleep. 1983;6:376–83.

    Article  CAS  PubMed  Google Scholar 

  79. Lo C-C, Chou T, Penzel T, Scammell TE, Strecker RE, Stanley HE, Ivanov PC. Common scale-invariant patterns of sleep-wake transitions across mammalian species. Proc Natl Acad Sci U S A. 2004;101:17545–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Chu-Shore J, Westover MB, Bianchi MT. Power law versus exponential state transition dynamics: application to sleep-wake architecture. PLoS One. 2010;5:e14204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Research grants received by KKG and VMK from the Cognitive Science Research Initiation program of the Department of Science and Technology, India (SR/CSI/110/2012 and SR/CSRI/102/2014), are acknowledged.

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Gulia, K.K., Aswathy, B.S., Kumar, V.M. (2021). Developmental Aspects of Sleep. In: Gozal, D., Kheirandish-Gozal, L. (eds) Pediatric Sleep Medicine. Springer, Cham. https://doi.org/10.1007/978-3-030-65574-7_10

Download citation

  • DOI: https://doi.org/10.1007/978-3-030-65574-7_10

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-030-65573-0

  • Online ISBN: 978-3-030-65574-7

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics