EEG and Sleep During Development

  • Raffaele FerriEmail author
  • Luana Novelli
  • Oliviero Bruni
Part of the Respiratory Medicine book series (RM)


In the pediatric age, quality and quantity of sleep change greatly together with its time organization, percentage of states of wakefulness, and electroencephalographic (EEG) activity patterns. Beside the development of sleep stages, this chapter analyzes in detail the maturation of several EEG phenomena during this period of life, such as sleep spindles, K complexes, slow-wave activity (SWA), sleep EEG scalp topography, and cyclic alternating pattern (CAP). Despite the careful analyses available in the literature on each of these activities, it is suggested that new studies should try to consider and integrate spindles, SWA, and CAP at once. A global vision of all the different significant aspects of sleep can provide a complete picture of the phenomenon, its relevance for the normal and pathological development, and its eventual usefulness for the clinical approach to developmental disorders.


  1. 1.
    Gaudreau H, Carrier J, Montplaisir J. Age-related modifications of NREM sleep EEG: from childhood to middle age. J Sleep Res. 2001;10(3):165–72.PubMedCrossRefGoogle Scholar
  2. 2.
    Curzi-Dascalova L. Waking and sleeping E.E.G. in normal babies before 6 months of age. Rev Electroencephalogr Neurophysiol Clin. 1977;7(3):316–26.PubMedCrossRefGoogle Scholar
  3. 3.
    Ellingson R. The EEGs of prematures and full-term newborns. In: Klass D, Daly D, editors. Current practice of clinical electroencephalography. New York: Raven; 1979. p. 149–77.Google Scholar
  4. 4.
    Louis J, Zhang JX, Revol M, Debilly G, Challamel MJ. Ontogenesis of nocturnal organization of sleep spindles: a longitudinal study during the first 6 months of life. Electroencephalogr Clin Neurophysiol. 1992;83(5):289–96.PubMedCrossRefGoogle Scholar
  5. 5.
    Schechtman VL, Harper RK, Harper RM. Distribution of slow wave EEG activity across the night in developing infants. Sleep. 1994;17(4):316–22.PubMedGoogle Scholar
  6. 6.
    Scher MS. Ontogeny of EEG-sleep from neonatal through infancy periods. Sleep Med. 2008;9:615–36.PubMedCrossRefGoogle Scholar
  7. 7.
    Anders TF, Keener M. Developmental course of nighttime sleep-wake patterns in full-term and premature infants during the first year of life. I. Sleep. 1985;8(3):173–92.PubMedGoogle Scholar
  8. 8.
    Montgomery-Downs HE, O’Brien LM, Gulliver TE, Gozal D. Polysomnographic characteristics in normal preschool and early school-aged children. Pediatrics. 2006;117:741–53.PubMedCrossRefGoogle Scholar
  9. 9.
    Iglowstein I, Jenni OG, Molinari L, Largo RH. Sleep duration from infancy to adolescence: reference values and generational trends. Pediatrics. 2003;111(2):302–7.PubMedCrossRefGoogle Scholar
  10. 10.
    Jenni OG, Borbely AA, Achermann P. Development of the nocturnal sleep electroencephalogram in human infants. Am J Physiol Regul Integr Comp Physiol. 2004;286:528–38.CrossRefGoogle Scholar
  11. 11.
    Sterman MB, Harper RM, Havens B, Hoppenbrouwers T, McGinty DJ, et al. Quantitative analysis of infant EEG development during quiet sleep. Electro­encephalogr Clin Neurophysiol. 1977;43(3):371–85.PubMedCrossRefGoogle Scholar
  12. 12.
    Samson-Dollfus D, Nogues B, Menard JF, Bertoldi-Lefever I, Geffroy D. Delta, theta, alpha and beta power spectrum of sleep electroencephalogram in infants aged two to eleven months. Sleep. 1983;6(4):376–83.PubMedGoogle Scholar
  13. 13.
    Feinberg I, Hibi S, Carlson VR. Changes in EEG amplitude during sleep with age. In: Nandy K, Sherwin I, editors. The aging brain and senile dementia. New York: Plenum Press; 1977. p. 86–98.Google Scholar
  14. 14.
    Berger H. Uber das Elektroencephalogram des Menschen. Arch Psychiatr Nervenkr. 1933;99:555–74.CrossRefGoogle Scholar
  15. 15.
    Loomis AL, Harvey EN, Hobart G. Potential rhythms of the cerebral cortex during sleep. Science. 1935;81:597–8.PubMedCrossRefGoogle Scholar
  16. 16.
    Steriade M. Cellular substrate of brain rhythms. In: Niedermeyer E, Lopes da Silva F, editors. Electro­encephalography: basic principles, clinical applications and related fields. Baltimore: Williams & Wilkins; 1993. p. 27–62.Google Scholar
  17. 17.
    Ellingson RJ, Peters JF. Development of EEG and daytime sleep patterns in low risk premature infants during the first year of life: longitudinal observations. Electroencephalogr Clin Neurophysiol. 1980;50(1–2):165–71.PubMedGoogle Scholar
  18. 18.
    Ellingson RJ, Peters JF. Development of EEG and daytime sleep patterns in normal full-term infant during the first 3 months of life: longitudinal observations. Electroencephalogr Clin Neurophysiol. 1980;49(1–2):112–24.PubMedGoogle Scholar
  19. 19.
    Sterman MB, McGinty DJ, Harper RM, Hoppenbrouwers T, Hodgman JE. Developmental comparison of sleep EEG power spectral patterns in infants at low and high risk for sudden death. Electroencephalogr Clin Neurophysiol. 1982;53:166–81.PubMedCrossRefGoogle Scholar
  20. 20.
    Tanguya PE, Ornitz EM, Kaplan A, Bozzo ES. Evolution of sleep spindles in childhood. Electroencephalogr Clin Neurophysiol. 1975;38:175–81.CrossRefGoogle Scholar
  21. 21.
    Shibagaki M, Kiyono S, Watanabe K. Spindle evolution in normal and mentally retarded children: a review. Sleep. 1982;5:47–57.PubMedGoogle Scholar
  22. 22.
    Nicolas A, Petit D, Rompre S, Montplaisir J. Sleep spindle characteristics in healthy subjects of different age groups. Clin Neurophysiol. 2001;12:521–7.CrossRefGoogle Scholar
  23. 23.
    Shinomiya S, Nagata K, Takahasi K, Masumura T. Development of sleep spindles in young children and adolescents. Clin Electroencephalogr. 1999;30:39–43.PubMedGoogle Scholar
  24. 24.
    Ellingson RJ. Development of sleep spindle bursts during the first year of life. Sleep. 1982;5:39–46.PubMedGoogle Scholar
  25. 25.
    Hughes JR. Development of sleep spindles in the first year of life. Clin Electroencephalogr. 1996;27:107–15.PubMedGoogle Scholar
  26. 26.
    Principe JC, Smith JR. Sleep spindle characteristics as a function of age. Sleep. 1982;5(1):73–84.PubMedGoogle Scholar
  27. 27.
    Scholle S, Zwacka G, Scholle HC. Sleep spindle evolution from infancy to adolescence. Clin Neurophysiol. 2007;118(7):1525–31.PubMedCrossRefGoogle Scholar
  28. 28.
    Gibbs EL, Lorimer FM, Gibbs FA. Clinical correlates of exceedingly fast activity in the electroencephalogram. Dis Nerv Syst. 1950;11(11):323–6.PubMedGoogle Scholar
  29. 29.
    Gibbs EL, Gibbs FA. Extreme spindles: correlation of electroencephalographic sleep pattern with mental retardation. Science. 1962;138:1106–7.PubMedCrossRefGoogle Scholar
  30. 30.
    Gibbs A, Gibbs EL. Atlas of electroencephalography. Volume III: neurological and psychiatric disorders. Reading: Frederic Addison-Wesley Publishing Co; 1964. p. 538.Google Scholar
  31. 31.
    Rechtschaffen A, Kales A, editors. A manual of standardized terminology, techniques and scoring system of sleep stages in human subjects. Los Angeles: Brain Information Service/Brain Research Institute, University of California; 1968.Google Scholar
  32. 32.
    Cash SS, Halgren E, Dehghani N, et al. The human K-complex represents an isolated cortical down-state. Science. 2009;324(5930):1084–7.PubMedCrossRefGoogle Scholar
  33. 33.
    Metcalf DR, Mondale J, Butler FK. Ontogenesis of spontaneous K-complexes. Psychophysiology. 1971;8(3):340–7.PubMedCrossRefGoogle Scholar
  34. 34.
    Niedermeyer E. Sleep and EEG. In: Niedermeyer E, Lopes da Silva F, editors. Electroencephalography. Basic principles, clinical applications and related fields. Batlimore: Urban and Schwarzenburg; 1982. p. 93–105.Google Scholar
  35. 35.
    Kubicki S, Scheuler W, Jobert M, Pastelak-Price M. The effect of age on sleep spindle and K complex density. EEG EMG Z Elektroenzephalogr Elektromyogr Verwandte Geb. 1989;20:59–63.PubMedGoogle Scholar
  36. 36.
    Wauquier A. Aging and changes in phasic events during sleep. Physiol Behav. 1993;54:803–6.PubMedCrossRefGoogle Scholar
  37. 37.
    Kellaway P. Ontogenetic evolution of the electrical activity of the brain in man and animal. Fourth International Congress of EEG Clinical Neuro­physiology. Acta Medica Belgica; 1957. p. 141–154.Google Scholar
  38. 38.
    Halasz P. K-complex, a reactive EEG graphoelement of NREM sleep: an old chap in a new garment. Sleep Med Rev. 2005;9(5):391–412.PubMedCrossRefGoogle Scholar
  39. 39.
    Dreyfus-Brisac C. Ontogenesis of sleep in human prematures after 32 weeks of conceptional age. Dev Psychobiol. 1970;3:91–121.PubMedCrossRefGoogle Scholar
  40. 40.
    Grigg-Damberger M, Gozal D, Marcus CL, et al. The visual scoring of sleep and arousal in infants and children. J Clin Sleep Med. 2007;3(2):201–40.PubMedGoogle Scholar
  41. 41.
    Smith JR, Karacan I, Yang M. Ontogeny of delta activity during human sleep. Electroencephalogr Clin Neurophysiol. 1977;43:229–37.PubMedCrossRefGoogle Scholar
  42. 42.
    Anders T, Emde R, Parmelee AH. A manual of standardized terminology, techniques, and criteria for scoring of state of sleep and wakefulness in newborn infants. Los Angeles: UCLA Brain Information; 1971.Google Scholar
  43. 43.
    Ficca G, Fagioli I, Salzarulo P. Sleep organization in the first year of life: developmental trends in the quiet sleep-paradoxical sleep cycle. J Sleep Res. 2000;9:1–4.PubMedCrossRefGoogle Scholar
  44. 44.
    Salzarulo P, Fagioli I, Salomon F. Maturation of sleep patterns in infants under continuous nutrition from birth. Acta Chir Scand Suppl. 1980;498:78–82.PubMedGoogle Scholar
  45. 45.
    Schechtman VL, Harper RM. The maturation of correlations between cardiac and respiratory measures across sleep states in normal infants. Sleep. 1992;15:41–7.PubMedGoogle Scholar
  46. 46.
    Campbell IG, Higgins LM, Trinidad JM, Richardson P, Feinberg I. The increase in longitudinally measured sleepiness across adolescence is related to the maturational decline in low-frequency EEG power. Sleep. 2007;30:1677–87.PubMedGoogle Scholar
  47. 47.
    Campbell IG, Darchia N, Khaw WY, Higgins LM, Feinberg I. Sleep EEG evidence of sex differences in adolescent brain maturation. Sleep. 2005;28:637–43.PubMedGoogle Scholar
  48. 48.
    Campbell IG, Feinberg I. Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation. Proc Natl Acad Sci USA. 2009;106:5177–80.PubMedCrossRefGoogle Scholar
  49. 49.
    Feinberg I, Higgins LM, Khaw WY, Campbell IG. The adolescent decline of NREM delta, an indicator of brain maturation, is linked to age and sex but not to pubertal stage. Am J Physiol Regul Integr Comp Physiol. 2006;291:1724–9.CrossRefGoogle Scholar
  50. 50.
    Feinberg I, Campbell IG. The onset of the adolescent delta power decline occurs after age 11 years: a comment on Tarokh and Carskadon. Sleep. 2010;33(6):737.PubMedGoogle Scholar
  51. 51.
    Jenni OG, Carskadon MA. Spectral analysis of the sleep electroencephalogram during adolescence. Sleep. 2004;27:774–83.PubMedGoogle Scholar
  52. 52.
    Jenni OG, Achermann P, Carskadon MA. Homeostatic sleep regulation in adolescents. Sleep. 2005;28(11):1446–54.PubMedGoogle Scholar
  53. 53.
    Jenni OG, Van RE, Carskadon MA. Regional differences of the sleep electroencephalogram in adolescents. J Sleep Res. 2005;14:141–7.PubMedCrossRefGoogle Scholar
  54. 54.
    De Gennaro L, Ferrara M, Curcio G, Cristiani R. Antero-posterior EEG changes during the wakefulness-sleep transition. Clin Neurophysiol. 2001;112:1901–11.PubMedCrossRefGoogle Scholar
  55. 55.
    De Gennaro L, Ferrara M, Curcio G, Cristiani R, Bertini M. Cortical EEG topography of REM onset: the posterior dominance of middle and high frequencies. Clin Neurophysiol. 2002;113:561–70.PubMedCrossRefGoogle Scholar
  56. 56.
    Landolt HP, Borbely AA. Age-dependent changes in sleep EEG topography. Clin Neurophysiol. 2001;112:369–77.PubMedCrossRefGoogle Scholar
  57. 57.
    Gasser T, Jennen-Steinmetz C, Sroka L, Verleger R, Mocks J. Development of the EEG of school-age children and adolescents. II. Topography. Electroence­phalogr Clin Neurophysiol. 1988;69:100–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Parrino L, Smerieri A, Rossi M, Terzano MG. Relationship of slow and rapid EEG components of CAP to ASDA arousals in normal sleep. Sleep. 2001;24:881–5.PubMedGoogle Scholar
  59. 59.
    Terzano MG, Parrino L, Smerieri A, et al. Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep. Sleep Med. 2001;2:537–53.PubMedCrossRefGoogle Scholar
  60. 60.
    Curzi-Dascalova L, Mirmiran M, editors. Manual of methods for recording and analyzing sleep-wakefulness states in preterm and full-term infant. Paris: Editions Inserm; 1996.Google Scholar
  61. 61.
    Louis J. Maturation du sommeil pendant le deux premières années de vie: aspects quantitatif, structurel et circadien. Neurophysiol Clin. 1998;28:477–91.PubMedCrossRefGoogle Scholar
  62. 62.
    Miano S, Villa MP, Blanco D, et al. Development of NREM sleep instability-continuity (cyclic alternating pattern) in healthy term infants aged 1 to 4 months. Sleep. 2009;32:83–90.PubMedGoogle Scholar
  63. 63.
    Ferri R, Bruni O, Miano S, et al. The time structure of the cyclic alternating pattern during sleep. Sleep. 2006;29(5):693–9.PubMedGoogle Scholar
  64. 64.
    Kahn E, Fisher C, Edwards A, Davis DM. 24-Hour sleep patterns: a comparison between 2- to 3-year-old and 4- to 6-year-old children. Arch Gen Psychiatry. 1973;29:380–5.PubMedCrossRefGoogle Scholar
  65. 65.
    Maron L, Rechtschaffen A, Wolpert EA. Sleep cycle during napping. Arch Gen Psychiatry. 1964;11:503–8.PubMedCrossRefGoogle Scholar
  66. 66.
    Bruni O, Ferri R, Miano S, et al. Sleep cyclic alternating pattern in normal preschool-aged children. Sleep. 2005;28:220–30.PubMedGoogle Scholar
  67. 67.
    Carskadon M, Keenan S, Dement WC. Nighttime sleep and daytime sleep tendency in preadolescents. In: Guilleminault C, editor. Sleep and its disorders in children. New York: Raven; 1987. p. 43–52.Google Scholar
  68. 68.
    Bruni O, Ferri R, Miano S, et al. Sleep cyclic alternating pattern in normal school-age children. Clin Neurophysiol. 2002;113:1806–14.PubMedCrossRefGoogle Scholar
  69. 69.
    Bruni O, Novelli L, Miano S, et al. Cyclic alternating pattern: a window into pediatric sleep. Sleep Med. 2010;11(7):628–36.PubMedCrossRefGoogle Scholar
  70. 70.
    Lopes MC, Rosa A, Roizenblatt S, et al. Cyclic alternating pattern in peripubertal children. Sleep. 2005;28(2):215–9.PubMedCrossRefGoogle Scholar
  71. 71.
    Parrino L, Boselli M, Spaggiari MC, Smerieri A, Terzano MG. Cyclic alternating pattern (CAP) in normal sleep: polysomnographic parameters in different age groups. Electroencephalogr Clin Neurophysiol. 1998;107:439–50.PubMedCrossRefGoogle Scholar
  72. 72.
    Terzano MG, Parrino L, Rosa A, Palomba V, Smerieri A. CAP and arousals in the structural development of sleep: an integrative perspective. Sleep Med. 2002;3:221–9.PubMedCrossRefGoogle Scholar
  73. 73.
    Ferri R, Bruni O, Miano S, Terzano MG. Topographic mapping of the spectral components of the “Cyclic Alternating Pattern” (CAP). Sleep Med. 2005;6:29–36.PubMedCrossRefGoogle Scholar
  74. 74.
    Ferri R, Bruni O, Miano S, Plazzi G, Terzano MG. All-night EEG power spectral analysis of the cyclic alternating pattern components in young adult subjects. Clin Neurophysiol. 2005;116:2429–40.PubMedCrossRefGoogle Scholar
  75. 75.
    Bruni O, Novelli L, Finotti E, et al. All-night EEG power spectral analysis of the cyclic alternating pattern at different ages. Clin Neurophysiol. 2009;120:248–56.PubMedCrossRefGoogle Scholar
  76. 76.
    Feinberg I, Thode Jr HC, Chugani HT, March JD. Gamma distribution model describes maturational curves for delta wave amplitude, cortical metabolic rate and synaptic density. J Theor Biol. 1990;142:149–61.PubMedCrossRefGoogle Scholar
  77. 77.
    Coble PA, Reynolds III CF, Kupfer DJ, Houck P. Electroencephalographic sleep of healthy children. Part II: findings using automated delta and REM sleep measurement methods. Sleep. 1987;10:551–62.PubMedGoogle Scholar
  78. 78.
    Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev. 2006;10(1):49–62.PubMedCrossRefGoogle Scholar
  79. 79.
    Takahashi Y, Kipnis DM, Daughaday WH. Growth hormone secretion during sleep. J Clin Invest. 1968;47:2079–90.PubMedCrossRefGoogle Scholar
  80. 80.
    Mirmiran M, Scholtens J, Van De Poll NE, et al. Effects of experimental suppression of active (REM) sleep during early development upon adult brain and behavior in the rat. Brain Res. 1983;283:277–86.PubMedGoogle Scholar
  81. 81.
    Mirmiran M, Van de Poll N, Corner MA, Van Oyen HG, Bour HL. Suppression of active sleep by chronic treatment with chlorimipramine during early postnatal development: effects upon sleep and behavior in the rat. Brain Res. 1981;204:129–46.PubMedCrossRefGoogle Scholar
  82. 82.
    Miano S, Bruni O, Elia M, et al. Sleep phenotypes of intellectual disability: a polysomnographic evaluation in subjects with Down syndrome and Fragile-X syndrome. Clin Neurophysiol. 2008;119:1242–7.PubMedCrossRefGoogle Scholar
  83. 83.
    Gigli GL, Grubar JC, Colognola RM, et al. Butoctamide hydrogen succinate and intensive learning sessions: effects on night sleep of Down’s syndrome patients. Sleep. 1987;10:563–9.PubMedGoogle Scholar
  84. 84.
    Grubar JC, Gigli GL, Colognola RM, et al. Sleep ­patterns of Down’s syndrome children: effects of butoctamide hydrogen succinate (BAHS) administration. Psychopharmacology (Berl). 1986;90:119–22.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  1. 1.Department of Neurology I.C.Oasi InstituteTroinaItaly
  2. 2.Department of NeuroscienceAfar-Fatebenefratelli HospitalRomeItaly
  3. 3.Department of Developmental Neurology and PsychiatrySapienza UniversityRomeItaly

Personalised recommendations