Dreaming and Offline Memory Consolidation

  • Erin J. WamsleyEmail author
Sleep (M Thorpy, M Billiard, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Sleep


Converging evidence suggests that dreaming is influenced by the consolidation of memory during sleep. Following encoding, recently formed memory traces are gradually stabilized and reorganized into a more permanent form of long-term storage. Sleep provides an optimal neurophysiological state to facilitate this process, allowing memory networks to be repeatedly reactivated in the absence of new sensory input. The process of memory reactivation and consolidation in the sleeping brain appears to influence conscious experience during sleep, contributing to dream content recalled on awakening. This article outlines several lines of evidence in support of this hypothesis, and responds to some common objections.


Sleep Dreaming Rapid eye movement Non-rapid eye movement Memory consolidation Offline processing Memory reactivation Replay Consciousness 


Compliance with Ethics Guidelines

Conflict of Interest

Erin J. Wamsley declares that the research described here was supported by National Institute of Mental Health grant R01-MH48832 (principal investigator Robert Stickgold), National Institutes of Health T32 training grant HL07901-10 to the Harvard Division of Sleep Medicine, and a KL2 Medical Research Investigator Training award (an appointed KL2 award) from Harvard Catalyst | The Harvard Clinical and Translational Science Center (National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health award 8KL2TR000168-05). She is also a principal investigator supported by an R21 grant from the National Institute of Mental Health (1R21MH098171-01A1) and has received grants from the BIAL Foundation. She has also received compensation for teaching a course at Harvard University.

Human and Animal Rights and Informed Consent

This article does not report original research findings. Some studies described here were performed in our laboratory at Beth Israel Deaconess Medical Center, where all human subjects signed informed consent prior to participation.


Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. 1.
    Plihal W, Born J. Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci. 1997;9:534–47.PubMedCrossRefGoogle Scholar
  2. 2.
    Payne JD, Tucker MA, Ellenbogen JM, Wamsley EJ, Walker MP, Schacter DL, et al. Memory for semantically related and unrelated declarative information: the benefit of sleep, the cost of wake. PLoS One. 2012;7:e33079.PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Tucker MA, Hirota Y, Wamsley EJ, Lau H, Chaklader A, Fishbein W. A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory. Neurobiol Learn Mem. 2006;86:241–7.PubMedCrossRefGoogle Scholar
  4. 4.
    Ellenbogen JM, Hulbert JC, Stickgold R, Dinges DF, Thompson-Schill SL. Interfering with theories of sleep and memory: sleep, declarative memory, and associative interference. Curr Biol. 2006;16:1290–4.PubMedCrossRefGoogle Scholar
  5. 5.
    Payne JD, Stickgold R, Swanberg K, Kensinger EA. Sleep preferentially enhances memory for emotional components of scenes. Psychol Sci. 2008;19:781.PubMedCrossRefGoogle Scholar
  6. 6.
    Hu P, Stylos-Allan M, Walker MP. Sleep facilitates consolidation of emotional declarative memory. Psychol Sci. 2006;17:891–8.PubMedCrossRefGoogle Scholar
  7. 7.
    Groch S, Wilhelm I, Diekelmann S, Born J. The role of REM sleep in the processing of emotional memories: Evidence from behavior and event-related potentials. Neurobiol Learn Mem. 2013;99:1–9.PubMedCrossRefGoogle Scholar
  8. 8.
    Walker MP, Brakefield T, Morgan A, Hobson JA, Stickgold R. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron. 2002;35:205–11.PubMedCrossRefGoogle Scholar
  9. 9.
    Nishida M, Walker MP. Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS One. 2007;2:e341.PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.
    Stickgold R, James L, Hobson JA. Visual discrimination learning requires sleep after training. Nat Neurosci. 2000;3:1237–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Nguyen ND, Tucker MA, Stickgold R, Wamsley EJ. Overnight sleep enhances hippocampus-dependent aspects of spatial memory. Sleep. 2013;36:1051–7.PubMedCentralPubMedGoogle Scholar
  12. 12.
    Wamsley EJ, Tucker MA, Payne JD, Stickgold R. A brief nap is beneficial for human route-learning: the role of navigation experience and EEG spectral power. Learn Mem. 2010;17:332.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Ferrara M, Iaria G, Tempesta D, Curcio G, Moroni F, Marzano C, et al. Sleep to find your way: the role of sleep in the consolidation of memory for navigation in humans. Hippocampus. 2008;18:844–51.PubMedCrossRefGoogle Scholar
  14. 14.
    Ferrara M, Iaria G, De Gennaro L, Guariglia C, Curcio G, Tempesta D, et al. The role of sleep in the consolidation of route learning in humans: a behavioural study. Brain Res Bull. 2006;71:4–9.PubMedCrossRefGoogle Scholar
  15. 15.
    Maury A. Le sommeil et les rêves. Paris: Didier; 1865.Google Scholar
  16. 16.
    de Saint-Denys H. Les rêves et les moyens de les diriger. Observations pratiques. Paris: Amyot; 1867.Google Scholar
  17. 17.
    Foulkes D, Rechtschaffen A. Presleep determinants of dream content: effect of two films. Percept Mot Skills. 1964;19:983–1005.PubMedCrossRefGoogle Scholar
  18. 18.
    Witkin HA, Lewis HB. Presleep experiences and dreams. New York: Random House; 1967.Google Scholar
  19. 19.
    Goodenough DR, Witkin HA, Koulack D, Cohen H. The effects of stress films on dream affect and on respiration and eye-movement activity during rapid-eye-movement sleep. Psychophysiology. 1975;12:313–20.PubMedCrossRefGoogle Scholar
  20. 20.
    Cartwright RD, Bernick N, Borowitz G. Effect of an erotic movie on the sleep and dreams of young men. Arch Gen Psychiatry. 1969;20:262–71.PubMedCrossRefGoogle Scholar
  21. 21.
    Wamsley EJ, Stickgold R. Incorporation of waking events into dreams. In: Stickgold R, Walter MP, editors. The neuroscience of sleep. London: Academic; 2009. p. 330–6.CrossRefGoogle Scholar
  22. 22.
    Dement WC, Kahn E, Roffwarg HP. The influence of the laboratory situation on the dreams of the experimental subject. J Nerv Ment Dis. 1965;140:119–31.PubMedCrossRefGoogle Scholar
  23. 23.
    Bowe-Anders C, Herman JH, Roffwarg HP. Effects of goggle-altered color perception on sleep. Percept Mot Skills. 1974;38:191–8.PubMedCrossRefGoogle Scholar
  24. 24.
    Tauber ES, Roffwarg HP, Herman J. The effects of longstanding perceptual alterations on the hallucinatory content of dreams. Psychophysiology. 1968;5:219.Google Scholar
  25. 25.
    Corsi-Cabrera M, Becker J, Garcia L, Ibarra R, Morales M, Souza M. Dream content after using visual inverting prisms. Percept Mot Skills. 1986;63:415–23.PubMedCrossRefGoogle Scholar
  26. 26.
    De Koninck J, Prevost F, Lortie-Lussier M. Vertical inversion of the visual field and REM sleep mentation. J Sleep Res. 1996;5:16–20.PubMedCrossRefGoogle Scholar
  27. 27.
    Fiss H, Kremer E, Litchman J. The mnemonic function of dreaming. Sleep Res. 1977;6:122.Google Scholar
  28. 28.
    De Koninck J, Christ G, Hébert G, Rinfret N. Language learning efficiency, dreams and REM sleep. Psychiatr J Univ Ott. 1990;15:91–2.PubMedGoogle Scholar
  29. 29.
    Stickgold R, Malia A, Maguire D, Roddenberry D, O’Connor M. Replaying the game: hypnagogic images in normals and amnesics. Science. 2000;290:350–3.PubMedCrossRefGoogle Scholar
  30. 30.
    Kusse C, Shaffii-LE Bourdiec A, Schrouff J, Matarazzo L, Maquet P. Experience-dependent induction of hypnagogic images during daytime naps: a combined behavioural and EEG study. J Sleep Res. 2012;21:10–20.PubMedCrossRefGoogle Scholar
  31. 31.
    Wamsley EJ, Perry K, Djonlagic I, Reaven LB, Stickgold R. Cognitive replay of visuomotor learning at sleep onset: temporal dynamics and relationship to task performance. Sleep. 2010;33:59–68.PubMedCentralPubMedGoogle Scholar
  32. 32.••
    Wamsley EJ, Tucker M, Payne JD, Benavides JA, Stickgold R. Dreaming of a learning task is associated with enhanced sleep-dependent memory consolidation. Curr Biol. 2010;20:850–5. This study demonstrates that participants who incorporate a pre-sleep spatial learning task into dreaming exhibit superior memory for the task following sleep. PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Solomonova E, Paquette T, Stenstrom P, Nielsen T. Different 10-day temporal patterns of dreams about sleep laboratory and virtual reality maze experiences: associates with temporally patterned changes in dreamed locus of control. Sleep Med. 2011;12 Suppl 1:S124.CrossRefGoogle Scholar
  34. 34.
    Wamsley EJ, Nguyen N, Tucker M, Olsen A, Stickgold R. EEG correlates of overnight memory consolidation in a virtual navigation task. Sleep. 2012;35(Abstr Suppl):A86Google Scholar
  35. 35.
    Fosse MJ, Fosse R, Hobson JA, Stickgold RJ. Dreaming and episodic memory: a functional dissociation? J Cogn Neurosci. 2003;15:1–9.PubMedCrossRefGoogle Scholar
  36. 36.
    Nielsen TA, Powell RA. Longitudinal dream incorporation: preliminary evidence of cognitive processing with an infradian period. Sleep Res. 1988;17:112.Google Scholar
  37. 37.
    Blagrove M, Fouquet NC, Henley-Einion JA, Pace-Schott EF, Davies AC, Neuschaffer JL, et al. Assessing the dream-lag effect for REM and NREM stage 2 dreams. PLoS One. 2011;6:e26708.PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Baylor GW, Cavallero C. Memory sources associated with REM and NREM dream reports throughout the night: a new look at the data. Sleep. 2001;24:165–70.PubMedGoogle Scholar
  39. 39.
    Cavallero C, Foulkes D, Hollifield M, Terry R. Memory sources of REM and NREM dreams. Sleep. 1990;13:449–55.PubMedGoogle Scholar
  40. 40.
    Wagner U, Gais S, Haider H, Verleger R, Born J. Sleep inspires insight. Nature. 2004;427:352–5.PubMedCrossRefGoogle Scholar
  41. 41.
    Ellenbogen JM, Hu PT, Payne JD, Titone D, Walker MP. Human relational memory requires time and sleep. Proc Natl Acad Sci U S A. 2007;104:7723.PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Alger SE, Lau H, Fishbein W. Slow wave sleep during a daytime nap is necessary for protection from subsequent interference and long-term retention. Neurobiol Learn Mem. 2012;98:188–96.PubMedCrossRefGoogle Scholar
  43. 43.
    Lau H, Alger SE, Fishbein W. Relational memory: a daytime nap facilitates the abstraction of general concepts. PLoS One. 2011;6:e27139.PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Euston DR, Tatsuno M, McNaughton BL. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science. 2007;318:1147–50.PubMedCrossRefGoogle Scholar
  45. 45.
    Bendor D, Wilson MA. Biasing the content of hippocampal replay during sleep. Nat Neurosci. 2012;15:1439–44.PubMedCrossRefGoogle Scholar
  46. 46.
    Ji D, Wilson MA. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci. 2006;10:100–7.PubMedCrossRefGoogle Scholar
  47. 47.
    Louie K, Wilson MA. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron. 2001;29:145–56.PubMedCrossRefGoogle Scholar
  48. 48.
    Lee AK, Wilson MA. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron. 2002;36:1183–94.PubMedCrossRefGoogle Scholar
  49. 49.
    Kudrimoti HS, Barnes CA, McNaughton BL. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 1999;19:4090–101.PubMedGoogle Scholar
  50. 50.
    Peigneux P, Laureys S, Fuchs S, Collette F, Perrin F, Reggers J, et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron. 2004;44:535–45.PubMedCrossRefGoogle Scholar
  51. 51.
    Laureys S, Peigneux P, Phillips C, Fuchs S, Degueldre C, Aerts J, et al. Experience-dependent changes in cerebral functional connectivity during human rapid eye movement sleep. Neuroscience. 2001;105:521–5.PubMedCrossRefGoogle Scholar
  52. 52.
    Wilson MA, McNaughton BL. Reactivation of hippocampal ensemble memories during sleep. Science. 1994;265:676–9.PubMedCrossRefGoogle Scholar
  53. 53.
    Verdone P. Temporal reference of manifest dream content. Percept Mot Skills. 1965;20:1253–68.PubMedCrossRefGoogle Scholar
  54. 54.
    O’Neill J, Pleydell-Bouverie B, Dupret D, Csicsvari J. Play it again: reactivation of waking experience and memory. Trends Neurosci. 2010;33:220–9.PubMedCrossRefGoogle Scholar
  55. 55.
    Vertes RP. Memory consolidation in sleep: dream or reality. Neuron. 2004;44:135–48.PubMedCrossRefGoogle Scholar
  56. 56.••
    Hartmann E. The dream always makes new connections: the dream is a creation, not a replay. Sleep Med Clin. 2010;5:241–8. In this theoretical paper, pioneering dream researcher Ernest Hartmann argues against a role for memory consolidation in dreaming. Several arguments raised here are addressed in the current paper. CrossRefGoogle Scholar
  57. 57.
    Payne JD, Schacter DL, Propper RE, Huang L-W, Wamsley EJ, Tucker MA, et al. The role of sleep in false memory formation. Neurobiol Learn Mem. 2009;92:327–34.PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Gómez RL, Bootzin RR, Nadel L. Naps promote abstraction in language-learning infants. Psychol Sci. 2006;17:670–4.PubMedCrossRefGoogle Scholar
  59. 59.••
    Tamminen J, Payne JD, Stickgold R, Wamsley EJ, Gaskell MG. Sleep spindle activity is associated with the integration of new memories and existing knowledge. J Neurosci. 2010;30:14356–60. This paper provides an excellent example of the role of sleep in integrating new information with established knowledge, rather than solely “strengthening” new memories in their original form. PubMedCentralPubMedCrossRefGoogle Scholar
  60. 60.
    Cai DJ, Mednick SA, Harrison EM, Kanady JC, Mednick SC. REM, not incubation, improves creativity by priming associative networks. Proc Natl Acad Sci U S A. 2009;106:10130.PubMedCentralPubMedCrossRefGoogle Scholar
  61. 61.
    McClelland JL, O’Reilly RC. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev. 1995;102:419–57Google Scholar
  62. 62.••
    Lewis PA, Durrant SJ. Overlapping memory replay during sleep builds cognitive schemata. Trends Cogn Sci. 2011;15:343–51. In this recent theoretical article, Lewis and Durrant propose an elegant model of sleep-dependent memory consolidation in which the simultaneous reactivation of related memories leads to the extraction of generalized knowledge. PubMedCrossRefGoogle Scholar
  63. 63.••
    Gupta AS, van der Meer MAA, Touretzky DS, Redish AD. Hippocampal replay is not a simple function of experience. Neuron. 2010;65:695–705. This important study from the rodent memory reactivation literature demonstrates that the socalled “replay” of memory during sleep should not be conceptualized as a veridical reiteration of waking experience. In fact, “replayed” sequences can include novel shortcut trajectories through the learned environment never experienced during wakefulness. PubMedCrossRefGoogle Scholar
  64. 64.
    Dement WC, Wolpert EA. The relation of eye movements, body motility, and external stimuli to dream content. J Exp Psychol. 1958;55:543–53.PubMedCrossRefGoogle Scholar
  65. 65.
    Hobson JA, McCarley RW. The brain as a dream state generator: an activation-synthesis hypothesis of the dream process. Am J Psychiatry. 1977;134:1335–48.PubMedGoogle Scholar
  66. 66.
    Flanagan O. Dreaming souls: sleep, dreams and the evolution of the conscious mind. New York: Oxford University Press; 1999.Google Scholar
  67. 67.
    Domhoff GW. The scientific study of dreams: neural networks, cognitive development, and content analysis. Washington: American Psychological Association; 2003.CrossRefGoogle Scholar
  68. 68.
    Crick F, Mitchison G. The function of dream sleep. Nature. 1983;304:111–4.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of PsychiatryHarvard Medical SchoolBostonUSA
  2. 2.Department of PsychologyFurman UniversityGreenvilleUSA

Personalised recommendations