Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Sleep-dependent memory triage: evolving generalization through selective processing

Nature Neuroscience volume 16, pages 139–145 (2013)Cite this article

Subjects

Abstract

The brain does not retain all the information it encodes in a day. Much is forgotten, and of those memories retained, their subsequent evolution can follow any of a number of pathways. Emerging data makes clear that sleep is a compelling candidate for performing many of these operations. But how does the sleeping brain know which information to preserve and which to forget? What should sleep do with that information it chooses to keep? For information that is retained, sleep can integrate it into existing memory networks, look for common patterns and distill overarching rules, or simply stabilize and strengthen the memory exactly as it was learned. We suggest such 'memory triage' lies at the heart of a sleep-dependent memory processing system that selects new information, in a discriminatory manner, and assimilates it into the brain's vast armamentarium of evolving knowledge, helping guide each organism through its own, unique life.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Selective memory consolidation.
Figure 2: Forms of memory evolution.
Figure 3: Examples of memory evolution.

References

  1. Stickgold, R. Sleep-dependent memory consolidation. Nature 437, 1272–1278 (2005).

    Article  CAS  PubMed  Google Scholar 

  2. Diekelmann, S. & Born, J. The memory function of sleep. Nat. Rev. Neurosci. 11, 114–126 (2010).

    Article  CAS  PubMed  Google Scholar 

  3. Maquet, P. The role of sleep in learning and memory. Science 294, 1048–1052 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Walker, M.P. & Stickgold, R. Sleep-dependent learning and memory consolidation. Neuron 44, 121–133 (2004).

    Article  CAS  PubMed  Google Scholar 

  5. Wang, G., Grone, B., Colas, D., Appelbaum, L. & Mourrain, P. Synaptic plasticity in sleep: learning, homeostasis and disease. Trends Neurosci. 34, 452–463 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Born, J. & Wagner, U. Awareness in memory: being explicit about the role of sleep. Trends Cogn. Sci. 8, 242–244 (2004).

    Article  PubMed  Google Scholar 

  7. Walker, M.P. et al. Sleep and the time course of motor skill learning. Learn. Mem. 10, 275–284 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Shadmehr, R. & Brashers-Krug, T. Functional stages in the formation of human long-term motor memory. J. Neurosci. 17, 409–419 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Ellenbogen, J.M., Hu, P.T., Payne, J.D., Titone, D. & Walker, M.P. Human relational memory requires time and sleep. Proc. Natl. Acad. Sci. USA 104, 7723–7728 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Walker, M.P., Liston, C., Hobson, J.A. & Stickgold, R. Cognitive flexibility across the sleep-wake cycle: REM-sleep enhancement of anagram problem solving. Brain Res. Cogn. Brain Res. 14, 317–324 (2002).

    Article  PubMed  Google Scholar 

  11. Mednick, S.C., Cai, D.J., Shuman, T., Anagnostaras, S. & Wixted, J.T. An opportunistic theory of cellular and systems consolidation. Trends Neurosci. 34, 504–514 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Muller, G.E. & Pilzecker, A. Experimentelle Beitrage zur Lehre von Gedachtnis. Z. Psychol. 1, 1–300 (1900).

    Google Scholar 

  13. Jenkins, J.G. & Dallenbach, K.M. Obliviscence during sleep and waking. Am. J. Psychol. 35, 605–612 (1924).

    Article  Google Scholar 

  14. Smith, C., Kitahama, K., Valatx, J.L. & Jouvet, M. Increased paradoxical sleep in mice during acquisition of a shock avoidance task. Brain Res. 77, 221–230 (1974).

    Article  CAS  PubMed  Google Scholar 

  15. Diekelmann, S. & Born, J. The memory function of sleep. Nat. Rev. Neurosci. 11, 114–126 (2010).

    CAS  PubMed  Google Scholar 

  16. Walker, M.P. & Stickgold, R. Sleep-dependent learning and memory consolidation. Neuron 44, 121–133 (2004).

    Article  CAS  PubMed  Google Scholar 

  17. Brawn, T.P., Fenn, K.M., Nusbaum, H.C. & Margoliash, D. Consolidating the effects of waking and sleep on motor-sequence learning. J. Neurosci. 30, 13977–13982 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Saletin, J.M. & Walker, M.P. Nocturnal mnemonics: sleep and hippocampal memory processing. Front. Neurol. 3, 59 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Wilhelm, I. et al. Sleep selectively enhances memory expected to be of future relevance. J. Neurosci. 31, 1563–1569 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hu, P., Stylos-Allan, M. & Walker, M.P. Sleep facilitates consolidation of emotional declarative memory. Psychol. Sci. 17, 891–898 (2006).

    Article  PubMed  Google Scholar 

  21. Atienza, M. & Cantero, J.L. Modulatory effects of emotion and sleep on recollection and familiarity. J. Sleep Res. 17, 285–294 (2008).

    Article  PubMed  Google Scholar 

  22. Nishida, M., Pearsall, J., Buckner, R.L. & Walker, M.P. REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb. Cortex 19, 1158–1166 (2009).

    Article  PubMed  Google Scholar 

  23. Wagner, U., Gais, S. & Born, J. Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn. Mem. 8, 112–119 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Baran, B., Pace-Schott, E.F., Ericson, C. & Spencer, R.M. Processing of emotional reactivity and emotional memory over sleep. J. Neurosci. 32, 1035–1042 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lewis, P.A., Cairney, S., Manning, L. & Critchley, H.D. The impact of overnight consolidation upon memory for emotional and neutral encoding contexts. Neuropsychologia 49, 2619–2629 (2011).

    Article  CAS  PubMed  Google Scholar 

  26. Payne, J.D., Stickgold, R., Swanberg, K. & Kensinger, E.A. Sleep preferentially enhances memory for emotional components of scenes. Psychol. Sci. 19, 781–788 (2008).

    Article  PubMed  Google Scholar 

  27. Fischer, S. & Born, J. Anticipated reward enhances offline learning during sleep. J. Exp. Psychol. Learn. Mem. Cogn. 35, 1586–1593 (2009).

    Article  PubMed  Google Scholar 

  28. van Dongen, E.V., Thielen, J.W., Takashima, A., Barth, M. & Fernandez, G. Sleep supports selective retention of associative memories based on relevance for future utilization. PLoS ONE 7, e43426 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Saletin, J.M., Goldstein, A.N. & Walker, M.P. The Role of Sleep in Directed Forgetting and Remembering of Human Memories. Cereb. Cortex 21, 2534–2541 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Anderson, M.C. & Huddleston, E. Towards a cognitive and neurobiological model of motivated forgetting. Nebr. Symp. Motiv. 58, 53–120 (2012).

    Article  PubMed  Google Scholar 

  31. Fischer, S., Diekelmann, S. & Born, J. Sleep's role in the processing of unwanted memories. J. Sleep Res. 20, 267–274 (2011).

    Article  PubMed  Google Scholar 

  32. Rauchs, G. et al. Sleep contributes to the strengthening of some memories over others, depending on hippocampal activity at learning. J. Neurosci. 31, 2563–2568 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Frey, S., Morris, R. & Petrides, M. A neuroanatomical method to assess the integrity of fibers of passage following ibotenate-induced damage to the central nervous system. Neurosci. Res. 28, 285–288 (1997).

    Article  CAS  PubMed  Google Scholar 

  34. Foster, D.J. & Wilson, M.A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440, 680–683 (2006).

    Article  CAS  PubMed  Google Scholar 

  35. Tambini, A., Ketz, N. & Davachi, L. Enhanced brain correlations during rest are related to memory for recent experiences. Neuron 65, 280–290 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Payne, J.D. & Kensinger, E.A. Sleep leads to changes in the emotional memory trace: evidence from fMRI. J. Cogn. Neurosci. 23, 1285–1297 (2011).

    Article  PubMed  Google Scholar 

  37. Yoo, S.-S., Gujar, N., Hu, P., Jolesz, F.A. & Walker, M.P. The human emotional brain without sleep–a prefrontal amygdala disconnect. Curr. Biol. 17, R877–R878 (2007).

    Article  CAS  PubMed  Google Scholar 

  38. Payne, J.D. et al. The role of sleep in false memory formation. Neurobiol. Learn. Mem. 92, 327–334 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Knutson, B. & Adcock, R.A. Remembrance of rewards past. Neuron 45, 331–332 (2005).

    Article  CAS  PubMed  Google Scholar 

  40. Wylie, G.R., Foxe, J.J. & Taylor, T.L. Forgetting as an active process: an FMRI investigation of item-method-directed forgetting. Cereb. Cortex 18, 670–682 (2008).

    Article  PubMed  Google Scholar 

  41. Shimamura, A.P. Episodic retrieval and the cortical binding of relational activity. Cogn. Affect. Behav. Neurosci. 11, 277–291 (2011).

    Article  PubMed  Google Scholar 

  42. Squire, L.R., Slater, P.C. & Chace, P.M. Retrograde amnesia: temporal gradient in very long term memory following electroconvulsive therapy. Science 187, 77–79 (1975).

    Article  CAS  PubMed  Google Scholar 

  43. Piaget, J. The Origins of Intelligence in Children (International Universities Press, New York, 1952).

  44. Tse, D. et al. Schemas and memory consolidation. Science 316, 76–82 (2007).

    Article  CAS  PubMed  Google Scholar 

  45. van Kesteren, M.T., Ruiter, D.J., Fernandez, G. & Henson, R.N. How schema and novelty augment memory formation. Trends Neurosci. 35, 211–219 (2012).

    Article  CAS  PubMed  Google Scholar 

  46. McGaugh, J.L. Memory–a century of consolidation. Science 287, 248–251 (2000).

    Article  CAS  PubMed  Google Scholar 

  47. Gaskell, M.G. & Dumay, N. Lexical competition and the acquisition of novel words. Cognition 89, 105–132 (2003).

    Article  PubMed  Google Scholar 

  48. Tamminen, J., Payne, J.D., Stickgold, R., Wamsley, E.J. & Gaskell, M.G. Sleep spindle activity is associated with the integration of new memories and existing knowledge. J. Neurosci. 30, 14356–14360 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Cai, D.J., Mednick, S.A., Harrison, E.M., Kanady, J.C. & Mednick, S.C. REM, not incubation, improves creativity by priming associative networks. Proc. Natl. Acad. Sci. USA 106, 10130–10134 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Wamsley, E.J., Tucker, M.A., Payne, J.D. & Stickgold, R. A brief nap is beneficial for human route-learning: the role of navigation experience and EEG spectral power. Learn. Mem. 17, 332–336 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Wamsley, E.J., Tucker, M., Payne, J.D., Benavides, J.A. & Stickgold, R. Dreaming of a learning task is associated with enhanced sleep-dependent memory consolidation. Curr. Biol. 20, 850–855 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Roediger, H.L. & McDermott, K.B. Creating false memories: remembering words not presented in lists. J. Exp. Psychol. Learn. Mem. Cogn. 21, 803–814 (1995).

    Article  Google Scholar 

  53. Diekelmann, S., Born, J. & Wagner, U. Sleep enhances false memories depending on general memory performance. Behav. Brain Res. 208, 425–429 (2010).

    Article  PubMed  Google Scholar 

  54. Fenn, K.M., Gallo, D.A., Margoliash, D., Roediger, H.L. III & Nusbaum, H.C. Reduced false memory after sleep. Learn. Mem. 16, 509–513 (2009).

    Article  PubMed  Google Scholar 

  55. Darsaud, A. et al. Does sleep promote false memories? J. Cogn. Neurosci. 23, 26–40 (2011).

    Article  PubMed  Google Scholar 

  56. Eichenbaum, H., Yonelinas, A.P. & Ranganath, C. The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30, 123–152 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Buckmaster, C.A., Eichenbaum, H., Amaral, D.G., Suzuki, W.A. & Rapp, P.R. Entorhinal cortex lesions disrupt the relational organization of memory in monkeys. J. Neurosci. 24, 9811–9825 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Gomez, R.L., Bootzin, R.R. & Nadel, L. Naps promote abstraction in language-learning infants. Psychol. Sci. 17, 670–674 (2006).

    Article  PubMed  Google Scholar 

  59. Hupbach, A., Gomez, R.L., Bootzin, R.R. & Nadel, L. Nap-dependent learning in infants. Dev. Sci. 12, 1007–1012 (2009).

    Article  PubMed  Google Scholar 

  60. Dusek, J.A. & Eichenbaum, H. The hippocampus and memory for orderly stimulus relations. Proc. Natl. Acad. Sci. USA 94, 7109–7114 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Durrant, S.J., Taylor, C., Cairney, S. & Lewis, P.A. Sleep-dependent consolidation of statistical learning. Neuropsychologia 49, 1322–1331 (2011).

    Article  PubMed  Google Scholar 

  62. Knowlton, B.J., Squire, L.R. & Gluck, M.A. Probabilistic classification learning in amnesia. Learn. Mem. 1, 106–120 (1994).

    CAS  PubMed  Google Scholar 

  63. Gluck, M.A., Shohamy, D. & Meyers, C.E. How do people solve the “weather prediction” task? Individual variability in strategies for probabilistic category learning. Learn. Mem. 9, 408–418 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Djonlagic, I. et al. Sleep enhances category learning. Learn. Mem. 16, 751–755 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Wagner, U., Gais, S., Haider, H., Verleger, R. & Born, J. Sleep inspires insight. Nature 427, 352–355 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. Mednick, S.A. The associative basis of the creative process. Psychol. Rev. 69, 220–232 (1962).

    Article  CAS  PubMed  Google Scholar 

  67. Stickgold, R., Scott, L., Rittenhouse, C. & Hobson, J.A. Sleep-induced changes in associative memory. J. Cogn. Neurosci. 11, 182–193 (1999).

    Article  CAS  PubMed  Google Scholar 

  68. Hasselmo, M.E. & Bower, J.M. Acetylcholine and memory. Trends Neurosci. 16, 218–222 (1993).

    Article  CAS  PubMed  Google Scholar 

  69. Smith, C. & Smith, D. Ingestion of ethanol just prior to sleep onset impairs memory for procedural but not declarative tasks. Sleep 26, 185–191 (2003).

    PubMed  Google Scholar 

  70. Lee, A.K. & Wilson, M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183–1194 (2002).

    Article  CAS  PubMed  Google Scholar 

  71. Wilson, M.A. & McNaughton, B.L. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676–679 (1994).

    Article  CAS  PubMed  Google Scholar 

  72. Louie, K. & Wilson, M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29, 145–156 (2001).

    Article  CAS  PubMed  Google Scholar 

  73. Giuditta, A. et al. The sequential hypothesis of the function of sleep. Behav. Brain Res. 69, 157–166 (1995).

    Article  CAS  PubMed  Google Scholar 

  74. Grosmark, A.D., Mizuseki, K., Pastalkova, E., Diba, K. & Buzsaki, G. REM sleep reorganizes hippocampal excitability. Neuron 75, 1001–1007 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Poe, G.R., Nitz, D.A., McNaughton, B.L. & Barnes, C.A. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res. 855, 176–180 (2000).

    Article  CAS  PubMed  Google Scholar 

  76. Stickgold, R., James, L. & Hobson, J.A. Visual discrimination learning requires sleep after training. Nat. Neurosci. 3, 1237–1238 (2000).

    Article  CAS  PubMed  Google Scholar 

  77. Schacter, D.L., Addis, D.R. & Buckner, R.L. Remembering the past to imagine the future: the prospective brain. Nat. Rev. Neurosci. 8, 657–661 (2007).

    Article  CAS  PubMed  Google Scholar 

  78. Schacter, D.L. & Addis, D.R. On the nature of medial temporal lobe contributions to the constructive simulation of future events. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1245–1253 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Support provided by US National Institutes of Health grants MH48832 and MH92638 (R.S.) and AG031164, MH093537 and DA031939 (M.P.W.). We thank E. Robertson, J. Chamberlain, M. Tucker, E. Wamsley, J. Saletin and I. Nieuwenhuis for discussions on these concepts and comments on this manuscript.

Author information

Authors and Affiliations

  1. Center for Sleep and Cognition, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts, USA

    Robert Stickgold

  2. Department of Psychology and Helen Wills Neuroscience Institute, Sleep and Neuroimaging Laboratory, University of California, Berkeley, Berkeley, California, USA.,

    Matthew P Walker

Authors
  1. Robert Stickgold
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew P Walker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Robert Stickgold or Matthew P Walker.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stickgold, R., Walker, M. Sleep-dependent memory triage: evolving generalization through selective processing. Nat Neurosci 16, 139–145 (2013). https://doi.org/10.1038/nn.3303

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3303

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing