Sleep Medicine Reviews
Volume 7, Issue 4 , Pages 321-334 , August 2003

Development of fetal and neonatal sleep and circadian rhythms

  • Majid Mirmiran

      Affiliations

    • Department of Pediatrics, School of Medicine, Stanford University, Amsterdam, The Netherlands
    • Netherlands Institute for Brain Research, Amsterdam, The Netherlands
  • ,
  • Yolanda G.H Maas

      Affiliations

    • Department of Visual System Analysis, University of Amsterdam, Amsterdam, The Netherlands
  • ,
  • Ronald L Ariagno

      Affiliations

    • Department of Pediatrics, School of Medicine, Stanford University, Amsterdam, The Netherlands

References 

  1. Mirmiran M. The function of fetal/neonatal rapid eye movement sleep. Behav Brain Res. 1995;69:13–22
  2. Prechtl HF. The organization of behavioral states and their dysfunction. Semin Perinatol. 1992;16:258–263
  3. Nijhuis JG, Prechtl HF, Martin CB, Bots RS. Are there behavioral states in the human fetus?. Early Hum Dev. 1982;6:177–195
  4. Mulder EJ, Visser GH, Bekedam DJ, Prechtl HF. Emergence of behavioral states in fetuses of type-1-diabetic women. Early Hum Dev. 1987;15:231–251
  5. Visser GHA, Poelmann-Weesjes G, Cohen TMN, Bekedam DJ. Fetal behavior at 30 to 32 weeks of gestation. Pediatr Res. 1987;22:655–658
  6. Curzi-Dascalova L, Peirano P, More-Kahn F. Development of sleep states in normal premature and full-term newborns. Dev Psychobiol. 1988;21:431–444
  7. Curzi-Dascalova L, Figueroa JM, Eiselt M, Christova E, Virassamy A, d'Allest AM. Sleep state organization in premature infants of less than 35 weeks' gestational age. Pediatr Res. 1993;34:624–628
  8. Anders, T, Emde, R, Parmelee, AH, A manual of standardized terminology, techniques and criteria for scoring states of sleep and wakefulness in newborn infants, Los Angeles, UCLA Brain Information Service, 1971
  9. 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
  10. de Weerd, A, van den Bossche, R, The development of sleep in neonates, Sleep Medicine Rev
  11. Kahn A, Dan B, Groswasser J, Franco P, Sottiaux M. Normal sleep architecture in infants and children. J Clin Neurophysiol. 1996;13:184–197
  12. Curzi-Dascalova, L, Mirmiran, M, Manual of methods for recording and analyzing sleep-wakefulness states in preterm and full-term infant, Paris, Les Éditions INSERM, 1996
  13. Scholle S, Schafer T. Atlas of states of sleep and wakefulness in infants and children. Somnologie. 1999;3:163–941
  14. Prechtl HF, Fargel JW, Weinmann HM, Bakker HH. Postures, motility and respiration of low-risk pre-term infants. Dev Med Child Neurol. 1979;21:3–27
  15. Pillai M, James D. Are the behavioral states of the newborn comparable to those of the fetus?. Early Hum Dev. 1990;22:39–49
  16. Groome LJ, Singh KP, Bentz LS, Holland SB, Atterbury JL, Swiber MJ. Temporal stability in the distribution of behavioral states for individual human fetuses. Early Hum Dev. 1997;48:187–197
  17. Groome LJ, Swiber MJ, Atterbury JL, Bentz LS, Holland SB. Similarities and differences in behavioral state organization during sleep periods in the perinatal infant before and after birth. Child Dev. 1997;68:1–11
  18. Giganti F, Fagioli I, Ficca G, Cioni G, Salzarulo P. Preterm infants prefer to be awake at night. Neuroscience Letters. 2001;312:55–57
  19. Coons S, Guilleminault C. Development of consolidated sleep and wakeful periods in relation to the day/night cycle in infancy. Dev Med Child Neurol. 1984;26:169–176
  20. Mirmiran M, Ariagno RL. Influence of light in the NICU on the development of circadian rhythms in preterm infants. Seminars in Perinatology. 2000;24:247–257
  21. Ariagno RL, Thoman EB, Boeddiker MA, Kugener B, Constantinou JC, Mirmiran M. Developmental care does not alter sleep and development of premature infants. Pediatrics. 1997;100:e9
  22. Anders T, Sostek AM. The use of time lapse video recording of sleep wake behavior. Psychophysiol. 1976;13:155–158
  23. Fagioli I, Salzarulo P. Sleep states development in the first year of life assessed through 24-h recordings. Early Hum Dev. 1982;6:215–228
  24. 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
  25. Louis J, Cannard C, Bastuji H, Challamel MJ. Sleep ontogenesis revisited. Sleep. 1997;20:323–333
  26. Salzarulo P, Fagioli I, Salomon F, Ricour C, Raimbault G, Ambrosi S. Sleep patterns in infants under continuous feeding from birth. Electroencephalogr Clin Neurophysiol. 1980;49:330–336
  27. Salzarulo P, Fagioli I. Post-natal development of sleep organization in man: speculations on the emergence of the “S process”. Neurophysiol Clin. 1992;22:107–115
  28. Apkarian P, Mirmiran M, Tijssen R. Effects of behavioral state on visual processing in neonates. Neuropediatrics. 1991;22:85–91
  29. Guilleminault C, Souquet M. Advances in perinatal neurology. Jamaca: Spectrum Publications, Inc; 1979;
  30. Scher MS, Steppe DA, Dahl RE, Asthana S, Guthrie RD. Comparison of EEG sleep measures in healthy full-term and preterm infants at matched conceptional ages. Sleep. 1992;15:442–448
  31. Peirano P, Fagioli II, Bes F, Salzarulo P. The role of slow-wave sleep on the duration of quiet sleep in infants. J Sleep Res. 1993;2:130–133
  32. 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;83:289–296
  33. Bes F, Schulz H, Navelet Y, Salzarulo P. The distribution of slow-wave sleep across the night: a comparison for infants, children, and adults. Sleep. 1991;14:5–12
  34. Fagioli I, Salzarulo P. Prior spontaneous nocturnal waking duration and EEG during quiet sleep in infants: an automatic analysis approach. Behav Brain Res. 1998;91:23–28
  35. Grether JK, Schulman J. Sudden infant death syndrome and birth weight. J Pediatr. 1989;114:561–567
  36. Malloy MH, Hoffman HJ. Prematurity, sudden infant death syndrome, and age of death. Pediatrics. 1995;96:464–471
  37. Malloy MH, Freeman DH. Birth weight- and gestational age-specific sudden infant death syndrome mortality: United States, 1991 versus 1995. Pediatrics. 2000;105:1227–1231
  38. Ariagno R, Mirmiran M. Sudden infant death syndrome: problems, progress, & possibilities. London: Arnold; 2001;
  39. Roffwarg HP, Muzio JN, Dement WC. Ontogenetic development of the human sleep-dream cycle. Science. 1966;152:604–619
  40. Jouvet-Mounier D, Astic L, Lacote D. Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Devel Psychobiol. 1970;2:216–239
  41. Anders T, Sadeh A, Appareddy V. Normal sleep in neonates and children. In:  Ferber R,  Kryger MH editor. Principles and practice of sleep medicine in the child. Philadelphia: Saunders; 1995;p. 7–18
  42. Mirmiran M, Corner M. Neuronal discharge patterns in the occipital cortex of developing rats during active and quiet sleep. Brain Res. 1982;255:37–48
  43. Van Someren EJ, Mirmiran M, Bos NP, Lamur A, Kumar A, Molenaar PC. Quantitative analysis of eye movements during REM-sleep in developing rats. Dev Psychobiol. 1990;23:55–61
  44. Birnholz JC. The development of human fetal eye movement patterns. Science. 1981;213:679–681
  45. Inoue M, Koyanagi T, Nakahara H, Hara K, Hori E, Nakano H. Functional development of human eye movement in utero assessed quantitatively with real-time ultrasound. Am J Obstet Gynecol. 1986;155:170–174
  46. Mirmiran M, Scholtens J, van de Poll NE, Uylings HB, van der Gugten J, Boer GJ. Effects of experimental suppression of active (REM) sleep during early development upon adult brain and behavior in the rat. Brain Res. 1983;283:277–286
  47. Mirmiran M, van de Poll NE, Corner MA, van Oyen HG, Bour HL. Suppression of active sleep by chronic treatment with chlorimipramine during early postnatal development: effects upon adult sleep and behavior in the rat. Brain Res. 1981;204:129–146
  48. Hilakivi L. Adult alcohol consumption after pharmacological intervention in neonatal sleep. Acta Physiol Scand Suppl. 1987;562:1–58
  49. Hilakivi LA, Hilakivi I, Kiianmaa K. Neonatal antidepressant administration suppresses concurrent active (REM) sleep and increases adult alcohol consumption in rats. Alcohol. 1987;339–343
  50. Vogel G, Neill D, Kors D, Hagler M. REM sleep abnormalities in a new animal model of endogenous depression. Neurosci Biobehav Rev. 1990;14:77–83
  51. Vogel G, Neill D, Hagler M, Kors D. A new animal model of endogenous depression: a summary of present findings. Neurosci Biobehav Rev. 1990;14:85–91
  52. Vogel G, Neill D, Hagler M, Kors D, Hartley P. Decreased intracranial self-stimulation in a new animal model of endogenous depression. Neurosci Biobehav Rev. 1990;14:65–68
  53. Mirmiran M. The importance of fetal/neonatal REM sleep. Eur J Obstet Gynecol Repro Biol. 1986;21:283–291
  54. De Boer S, Mirmiran M, Van Haaren F, Louwerse A, van de Poll NE. Neurobehavioral teratogenic effects of clomipramine and alpha-methyldopa. Neurotoxicol Teratol. 1989;11:77–84
  55. Vogel GW, Feng P, Kinney GG. Ontogeny of REM sleep in rats: possible implications for endogenous depression. Physiol Behav. 2000;68:453–461
  56. Neill D, Vogel G, Hagler M, Kors D, Hennessey A. Diminished sexual activity in a new animal model of endogenous depression. Neurosci Biobehav Rev. 1990;14:73–76
  57. Hilakivi LA, Hilakivi I. Increased adult behavioral “despair” in rats neonatally exposed to desipramine or zimeldine: an animal model of depression?. Pharmacol Biochem Behav. 1987;28:367–369
  58. Hilakivi LA, Sinclair JD, Hilakivi IT. Effects of neonatal treatment with clomipramine on adult ethanol related behavior in the rat. Brain Res. 1984;317:129–132
  59. Mirmiran M, Feenstra MG, Dijcks FA, Bos NP, Van Haaren F. Functional deprivation of noradrenaline neurotransmission: effects of clonidine on brain development. Prog Brain Res. 1988;73:159–172
  60. Mirmiran M, Dijcks FA, Bos NP, Gorter JA, Van der Werf D. Cortical neuron sensitivity to neurotransmitters following neonatal noradrenaline depletion. Int J Dev Neurosci. 1990;8:217–221
  61. Gorter JA, Kamphuis W, Huisman E, Bos NP, Mirmiran M. Neonatal clonidine treatment results in long-lasting changes in noradrenaline sensitivity and kindling epileptogenesis. Brain Res. 1990;535:62–66
  62. Mirmiran M, Uylings HB, Corner MA. Pharmacological suppression of REM sleep prior to weaning counteracts the effectiveness of subsequent environmental enrichment on cortical growth in rats. Brain Res. 1983;283:102–105
  63. Gorter JA, Veerman M, Mirmiran M, Bos NP, Corner MA. Spectral analysis of the electroencephalogram in neonatal rats chronically treated with the NMDA antagonist MK-801. Dev Brain Res. 1991;64:37–41
  64. Davenne D, Adrien J. Lesion of the ponto-geniculo-occipital pathways in kittens. I. Effects on sleep and on unitary discharge of the lateral geniculate nucleus. Brain Res. 1987;409:1–9
  65. Marks GA, Shaffery JP, Oksenberg A, Speciale SG, Roffwarg HP. A functional role for REM sleep in brain maturation. Behav Brain Res. 1995;69:1–11
  66. Shaffery JP, Roffwarg HP, Speciale SG, Marks GA. Ponto-geniculo-occipital-wave suppression amplifies lateral geniculate nucleus cell-size changes in monocularly deprived kittens. Brain Res Dev Brain Res. 1999;114:109–119
  67. Oksenberg A, Shaffery JP, Marks GA, Speciale SG, Mihailoff G, Roffwarg HP. Rapid eye movement sleep deprivation in kittens amplifies LGN cell-size disparity induced by monocular deprivation. Dev Brain Res. 1996;97:51–61
  68. Frank MG, Issa NP, Stryker MP. Sleep enhances plasticity in the developing visual cortex. Neuron. 2001;30:275–287
  69. Maquet P, Laureys S, Peigneux P, Fuchs S, Petiau C, Phillips C. Experience-dependent changes in cerebral activation during human REM sleep. Nature Neurosci. 2000;3:831–836
  70. Maquet P. Functional neuroimaging of normal human sleep by positron emission tomography. J Sleep Res. 2000;9:207–231
  71. Stickgold R, James L, Hobson JA. Visual discrimination learning requires sleep after training. Nature Neurosci. 2000;3:1237–1238
  72. Smith C. Sleep states and memory processes. Behav Brain Res. 1995;69:137–145
  73. Skaggs WE, McNaughton BL. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996;271:1870–1873
  74. Wilson MA, McNaughton BL. Reactivation of hippocampal ensemble memories during sleep. Science. 1994;265:676–679
  75. Rechtschaffen A, Bergmann BM, Everson CA, Kushida CA, Gilliland MA. Sleep deprivation in the rat: X. Integration and discussion of the findings. Sleep. 1989;12:68–87
  76. Mirmiran M, Kok JH, Boer K, Wolf H. Perinatal development of human circadian rhythms: role of the foetal biological clock. Neurosci Biobehav Rev. 1992;16:371–378
  77. Seron-Ferre M, Torres-Farfan C, Forcelledo ML, Valenzuela GJ. The development of circadian rhythms in the fetus and neonate. Semin Perinatol. 2001;25:363–370
  78. Reppert SM, Schwartz WJ. Functional activity of the suprachiasmatic nucleus in the fetal primate. Neurosci Lett. 1984;46:145–149
  79. Rivkees SA, Hofman PL, Fortman J. Newborn primate infants are entrained by low intensity lighting. Proc Natl Acad Sci. 1997;94:292–297
  80. Hao HP, Rivkees SA. The circadian clock of very premature primate infants is responsive to light. Proc Natl Acad Sci USA. 1999;96:2426–2429
  81. Mirmiran M, Lunshof S. Perinatal development of human circadian rhythms. Prog Brain Res. 1996;111:217–226
  82. Lunshof S, Boer K, Wolf H, van Hoffen G, Bayram N, Mirmiran M. Fetal and maternal diurnal rhythms during the third trimester of normal pregnancy: outcomes of computerized analysis of continuous 24-hr fetal heart rate recordings. Am J Obst Gyncol. 1998;178:247–254
  83. Seron-Ferre M, Riffo R, Valenzuela GJ, Germain AM. Twenty-four-hour pattern of cortisol in the human fetus at term. Am J Obstet Gynecol. 2001;184:1278–1283
  84. Lunshof S, Boer K, van Hoffen G, Wolf H, Mirmiran M. The diurnal rhythm in fetal heart rate in a twin pregnancy with discordant anencephaly: comparison with three normal twin pregnancies. Early Hum Dev. 1997;48:47–57
  85. Petersen SA, Anderson ES, Lodemore M, Rawson D, Wailoo MP. Sleeping position and rectal temperature. Arch Dis Child. 1991;66:976–979
  86. Lodemore MR, Petersen SA, Wailoo MP. Factors affecting the development of night time temperature rhythms. Arch Dis Child. 1992;67:1259–1261
  87. Recio R, Riguez RM, Buxton OM, Challet E. Synchronizing circadian-rhythms in early infancy. Medical Hypotheses. 1997;49:229–234
  88. Illnerova H, Buresova M, Presl J. Melatonin rhythm in human milk. J Clin Endocrinol Metab. 1993;77:838–841
  89. McGraw K, Hoffmann R, Harker C, Herman JH. The development of circadian rhythms in a human infant. Sleep. 1999;22:303–310
  90. Sadeh A. Sleep and melatonin in infants: a preliminary study. Sleep. 1997;20:185–191
  91. Sitka U, Weinert D, Berle K, Rumler W, Schuh J. Investigations of the rhythmic function of heart rate, blood pressure and temperature in neonates. Eur J Pediatr. 1994;153:117–122
  92. Lohr B, Siegmund R. Ultradian and circadian rhythms of sleep-wake and food-intake behavior during early infancy. Chronobiology International. 1999;129–148
  93. Mirmiran M, Bernardo L, Jenkins SL, Ma XH, Brenna JT, Nathanielsz PW. Growth, neurobehavioral and circadian rhythm development in newborn baboons. Pediatr Res. 2001;49:673–677
  94. Kennaway DJ, Stamp GE, Goble FC. Development of melatonin production in infants and the impact of prematurity. J Clin Endocrinol Metab. 1992;75:367–369
  95. Jaldoalba F, Munozhoyos A, Molinacarballo A, Molinafont JA, Acunacastroviejo D. Light Deprivation Increases Plasma-Levels of Melatonin During the 1st 72-H of Life in Human Infants. Acta Endocrinologica. 1993;442–445
  96. Mantagos S, Moustogiannis A, Makri M, Vagenakis A. The effect of light on plasma melatonin levels in premature infants. J Pediatr Endocrinol Metab. 1996;9:387–392
  97. Mantagos S, Moustogiannis A, Vagenakis AG. Diurnal-variation of plasma-cortisol levels in infancy. J Ped Endocrin Metab. 1998;11:549–553
  98. Antonini SR, Jorge SM, Moreira AC. The emergence of salivary cortisol circadian rhythm and its relationship to sleep activity in preterm infants. Clin Endocrinol (Oxf). 2000;52:423–426
  99. Mirmiran M, Kok JH, de Kleine MJ, Koppe JG, Overdijk J, Witting W. Circadian rhythms in preterm infants: a preliminary study. Early Hum Dev. 1990;23:139–146
  100. Mann NP, Haddow R, Stokes L, Goodley S, Rutter N. Effect of night and day on preterm infants in a newborn nursery: randomized trial. Br Med J [Clin Res]. 1986;293:1265–1267
  101. Mirmiran M, Kok JH. Circadian rhythms in early human development. Early Hum Dev. 1991;26:121–128
  102. Tenreiro S, Dowse HB, D'Souza S, Minors D, Chiswick M, Simms D. The development of ultradian and circadian rhythms in premature babies maintained in constant conditions. Early Hum Dev. 1991;27:33–52
  103. McMillen IC, Kok JSM, Adamson TM, Deayton JM, Nowak R. Development of circadian sleep-wake rhythms in preterm and full-term infants. Pediatr Res. 1991;29:381–384
  104. Shimada M, Segawa M, Higurashi M, Akamatsu H. Development of the sleep and wakefulness rhythm in preterm infants discharged from a neonatal care unit. Pediat Res. 1993;33:159–163
  105. Shimada M, Takahashi K, Segawa M, Higurashi M, Samejim M, Horiuchi K. Emerging and entraining patterns of the sleep-wake rhythm in preterm and term infants. Brain & Development. 1999;21:468–473
  106. American Academy of Pediatrics and The American College of Obstetricians and Gynecologists, Guidelines for Perinatal Care

 Supported by NIH grant HD 35754.

PII: S1087-0792(02)90243-1

doi: 10.1053/smrv.2002.0243

Sleep Medicine Reviews
Volume 7, Issue 4 , Pages 321-334 , August 2003