Sleep Medicine Reviews
Volume 5, Issue 6 , Pages 477-490 , December 2001

Learning and sleep: the sequential hypothesis

  • M.V. Ambrosini

      Affiliations

    • Dipartimento di Medicina Sperimentale e Scienze Biochimiche, Università di Perugia, Via del Giochetto, Perugia, 06122
    • ,
  • A. Giuditta

      Affiliations

    • Dipartimento di Fisiologia Generale e Ambientale, Via Mezzocannone 8, Napoli, 80134, Italy

References 

  1. Jenkins J, Dallenbach K. Obliviscence during sleep and waking. Am J Psychol. 1924;35:605–612
  2. Crick F, Mitchison G. REM sleep and neural nets. Behav Brain Res. 1995;69:147–155
  3. Hennevin E. Hennevin E Processing of learned information in paradoxical sleep: relevance for memory. Behav Brain Res. 1995;69:125–135
  4. Horne JA, McGrath MJ. The consolidation hypothesis for REM sleep function: stress and other confounding factors – a review. Biol Psychol. 1984;18:165–184
  5. Fishbein W, Gutwein BM. Paradoxical sleep and memory storage processes. Behav Biol. 1977;19:425–464
  6. Giuditta A. A sequential hypothesis for the function of sleep. In:  Koella WP,  Ruther E,  Schulz H editor. Sleep '84. Stuttgart: Fischer Verlag; 1985;p. 222–224
  7. Giuditta A. Giuditta A The sequential hypothesis of the function of sleep. Behav Brain Res. 1995;69:157–166
  8. Greenberg R, Pearlman C. Cutting the REM nerve: an approach to the adaptive function of REM sleep. Perspect Biol Med. 1974;17:513–521
  9. McGrath MJ, Cohen DB. REM sleep facilitation of adaptive waking behavior: a review of the literature. Psychol Bull. 1978;85:24–57
  10. Pearlman CA. REM sleep and information processing: evidence from animal studies,. Neurosci Biobehav Rev. 1979;3:57–68
  11. Smith C. Sleep states and learning: a review of the animal literature. Neurosci Biobehav Rev. 1985;9:157–168
  12. Smith C. Sleep states and memory processes. Behav Brain Res. 1995;69:137–145
  13. Smith C. Sleep states, memory processes and synaptic plasticity. Behav Brain Res. 1996;78:49–56
  14. Vertes RP, Eastman KE. The case against memory consolidation in REM sleep. Behav Brain Sci. 2001;
  15. Giuditta A. The biochemistry of sleep. In:  Davidson AN editors. Biochemical Correlates of Brain Structure and Function. New York: Academic Press; 1977;p. 293–337
  16. Gardner-Medwin AR, Kaul S. Possible mechanisms for reducing memory confusion during sleep. Behav Brain Res. 1995;69:167–175
  17. Ficca G, Lombardo P, Rossi L, Salzaulo P. Morning recall of verbal material depends on prior sleep organization. Behav Brain Res. 2000;112:159–163
  18. Gais S, Plihal W, Wagner U, Born J. Early sleep triggers memory for early visual discrimination skills. Nat Neurosci. 2000;3:1335–1339
  19. Stickgold R, James L, Hobson JA. Visual discrimination learning requires sleep after training. Nat Neurosci. 2000;3:1237–1238
  20. Stickgold R, Whidbee D, Schirmer B, Patel V, Hobson JA. Visual discrimination task improvement: a multi-step process occurring during sleep. J Cogn Neurosci. 2000;12:246–254
  21. Pavlides C, Winson J. Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes. J Neurosci. 1989;9:2907–2918
  22. Chrobak JJ, Buzsáki G. Selective activation of deep layer (V–VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat. J Neurosci. 1994;14:6160–6170
  23. Nádasdy Z, Hiase H, Czurko A, Csicsvari J, Buzsaki G. Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci. 1999;19:9497–9507
  24. Chrobak JJ, Lorincz A, Buzsáki G. Physiological patterns in the hippocampo-entorhinal cortex system. Hippocampus. 2000;10:457–465
  25. Wilson MA, McNaughton B. Reactivation of hippocampal ensemble memories during sleep. Science. 1994;265:676–679
  26. Skaggs WE, McNaughton B. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science. 1996;271:1870–1873
  27. Kudrimoti HS, Barnes CA, McNaughton BL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 1999;19:4090–4101
  28. Poe GR, Nitz DA, McNaughton BL, Barnes CA. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res. 2000;855:176–180
  29. Lucero M. Lengthening of REM sleep duration consecutive to learning in the rat. Brain Res. 1970;20:319–322
  30. Leconte P, Hennevin E. Augmentation de la durée de sommeil paradoxal consécutif à un apprentissage chez le rat. C R Acad Sci. 1971;273:86–88
  31. Leconte P, Hennevin E. Caractéristiques temporelles de l'augmentation de sommeil paradoxal consécutif à l'apprentissage chez le rat. Physiol Behav. 1973;11:677–686
  32. McGaugh JL. Time-dependent processes in memory storage. Science. 1966;153:1351–1358
  33. Kandel ER, Pittenger C. The past, the future and the biology of memory storage. Phil Trans R Soc. 354. 1999; p. 2027–2052
  34. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science. 1986;234:1249–1254
  35. McGaugh JL. Memory-a century of consolidation. Science. 2000;287:248–251
  36. Squire LR, Slater PC, Chace PM. Retrograde amnesia: temporal gradient in very long term memory following electroconvulsive therapy. Science. 1975;187:77–79
  37. Nader K, Schafe GE, Le Doux JE. Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature. 2000;406:722–726
  38. Smith C, Gisquet-Verrier P. Paradoxical sleep deprivation and sleep recording following training in a brightness discrimination avoidance task in Sprague-Dawley rats: paradoxical effects. Neurobiol Learn Memory. 1996;66:283–294
  39. Giuditta A, Perrone Capano C, Grassi Zucconi G. The neurochemical study of sleep. In:  Lajtha A editors. Handbook of Neurochemistry. 8:New York: Plenum Press; 1984;p. 443–476
  40. Rideout BE. Non-REM sleep as a source of learning deficits induced by REM sleep deprivation. Physiol Behav. 1979;22:1043–1047
  41. Reich P, Geyer SJ, Karnowski ML. Metabolism of brain during sleep and wakefulness. J Neurochem. 1972;19:487–497
  42. Ambrosini MV, Langella M, Gironi Canevale UA, Giuditta A. The sequential hypothesis of sleep function. III. The structure of postacquisition sleep in learning and non learning rats. Physiol Behav. 1992;51:217–226
  43. Langella M, Colarieti L, Ambrosini MV, Giuditta A. The sequential hypothesis of sleep function. IV. A correlative analysis among behavioral, biochemical and sleep variables in learning and non learning rats. Physiol Behav. 1992;51:227–238
  44. Ambrosini MV, Sadile AG, Gironi Carnevale UA, Mattiacio M, Giuditta A. The sequential hypothesis on sleep function. I. Evidence that the structure of sleep depends on the nature of previous waking experience. Physiol Behav. 1988;43:325–337
  45. Ambrosini MV, Sadile AG, Gironi Carnevale UA, Mattiacio M, Giuditta A. The sequential hypothesis on sleep function. II. A correlative study between sleep variables and newly synthesized brain DNA. Physiol Behav. 1988;43:339–350
  46. Ambrosini MV, Bruschelli G, Mariucci G, Mandile P, Giuditta A. Post-trial sleep in old rats trained for a two-way active avoidance task. Physiol Behav. 1997;62:773–778
  47. Montagnese P, Mandile P, Vescia S, Sadile AG, Giuditta A. Long-term habituation to spatial novelty modifies post-trial synchronized sleep followed by paradoxical sleep in rats. Brain Res Bull. 1993;32:503–508
  48. Ambrosini MV, Mariucci G, Bruschelli G, Colarieti L, Giuditta A. The sequential hypothesis of sleep function. V. Lenghtening of post-trial SS episodes in reminiscent rats. Physiol Behav. 1995;58:1043–1049
  49. Gisquet-Verrier P, Alexinsky T. Long-term spontaneous improvement of performance is related to the strength of the initial training: theoretical implications. Behav Neur Biol. 1990;53:298–304
  50. Destrade C. Relationships between paradoxical sleep and time-dependent improvement of performance in BALB/c mice. Neurosci Lett. 1978;7:239–244
  51. Kitahama K, Valatx JL, Jouvet M. Paradoxical sleep deprivation and performance of an active avoidance task: impairment in C57BR mice and no effect in C57BL/6 mice. Physiol Behav. 1981;27:41–50
  52. Mandile P, Vescia S, Montagnese P, Rouano F, Giuditta A. Characterization of transition sleep episodes in baseline EEG recordings of adult rats. Physiol Behav. 1996;60:1435–1439
  53. Vescia S, Mandile P, Montagnese P, Romano F, Cataldo G, Cotugno M, et al. Baseline transition sleep and associated sleep episodes are related to the learning ability of rats. Physiol Behav. 1996;60:1513–1525
  54. Ambrosini MV, Mariucci G, Colarieti L, Bruschelli G, Carobi C, Giuditta A. The structure of sleep is related to the learning ability of rats. Eur J Neurosci. 1993;5:269–275
  55. Mandile P, Vescia S, Montagnese P, Piscopo S, Cotugno M, Giuditta A. Post-trial sleep sequences including transition sleep are involved in avoidance learning of adult rats. Behav Brain Res. 2000;112:23–31
  56. Piscopo S, Mandile P, Montagnese P, Cotugno M, Giuditta A, Vescia S. Identification of trains of sleep sequences in adult rats. Behav Brain Res. 2001;119:93–101
  57. Piscopo S, Mandile P, Montagnese P, Cotugro M, Giuditta A, Vescia S. Trains of sleep sequences are indices of learning capacity in rats. Behav Brain Res. 2001;120:13–21
  58. Datta S. Avoidance task training potentiates phasic pontine-wave density in the rat: a mechanism for sleep-dependent plasticity. J Neurosci. 2000;20:8607–8613
  59. Smith C. The relationship between sleep and cognition in humans. Sleep Med Rev. 2001;5:491–506
  60. Buzsáki G. Two-stage model of memory trace formation: a role for “noisy” brain states. Neurosci. 1989;31:551–570
  61. Buzsáki G. Memory consolidation during sleep: a neurophysiological perspective. J Sleep Res. 1998;7:17–23
  62. Steriade M. Corticothalamic resonance, states of vigilance and mentation. Neurosci. 2000;101:243–276
  63. Sejnowski TJ, Destexhe A. Why do we sleep?. Brain Res. 2000;886:208–223
  64. Cirelli C, Tononi G. On the functional significance of c-fos induction during the sleep-waking cycle. Sleep. 2000;23:453–469
  65. Cirelli C, Tononi G. Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system. J Neurosci. 2000;20:9187–9194
  66. Kennedy C, Gillin JC, Mendelson W. Local cerebral glucose utilization in non-rapid eye movement sleep. Nature. 1982;297:325–327
  67. Stickgold R. Sleep: off-line memory reprocessing. Trends Cogn Sci. 1998;2:484–492
  68. Winson J. The biology and function of rapid eye movement sleep. Curr Opin Neurobiol. 1993;3:243–248
  69. Maquet P, Lavreys S, Peigneux P. Experience-dependent changes incerebral activation during human REM sleep. Nat Neurosci. 2000;3:831–836
  70. Ribeiro S, Goyal V, Mello CV, Pavlides C. Brain gene expression during REM sleep depends on prior waking experience. Learn Mem. 1999;6:500–508
  71. Stickgold R, Scott L, Rittehouse C, Hobson JA. Sleep-induced changes in associative memory. J Cogn Neurosci. 1999;11:182–193
  72. Shaffery JP, Oksenberg A, Marks GA, Speciale SG, Mihailoff G, Roffwarg HP. REM sleep deprivation in monocularly occluded kittens reduces the size of cells in LGN monocular segment. Sleep. 1998;21:837–845

PII: S1087-0792(01)90180-7

doi: 10.1053/smrv.2001.0180

Sleep Medicine Reviews
Volume 5, Issue 6 , Pages 477-490 , December 2001

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