Sleep-dependent memory consolidation

Abstract

The concept of ‘sleeping on a problem’ is familiar to most of us. But with myriad stages of sleep, forms of memory and processes of memory encoding and consolidation, sorting out how sleep contributes to memory has been anything but straightforward. Nevertheless, converging evidence, from the molecular to the phenomenological, leaves little doubt that offline memory reprocessing during sleep is an important component of how our memories are formed and ultimately shaped.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1
Figure 2
Figure 3: Sleep-dependent consolidation of procedural memories.
Figure 4: Fit of data to exponential model of motor learning.
Figure 5: Complex cognitive procedural learning.
Figure 6: Experience-dependent upregulation of the synaptic plasticity related immediate early gene zif-268 during periods of wakefulness, SWS and REM sleep in the rat.

References

  1. 1

    Institutes of Oratory. Quintilian 〈http://lee.engl.iastate.edu/11/chapter2.html〉 (2004).

  2. 2

    Karni, A., Tanne, D., Rubenstein, B. S., Askenasy, J. J. M. & Sagi, D. Dependence on REM Sleep of overnight improvement of a perceptual skill. Science 265, 679–682 (1994).

    ADS  CAS  Article  Google Scholar 

  3. 3

    Stickgold, R. & Walker, M. P. Sleep and memory: the ongoing debate. Sleep 28, 1225–1227 (2005).

    Article  Google Scholar 

  4. 4

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

    CAS  Article  Google Scholar 

  5. 5

    Vertes, R. P. & Siegel, J. M. Time for the sleep community to take a critical look at the purported role of sleep in memory processing. Sleep 28, 1228–1229 (2005).

    Article  Google Scholar 

  6. 6

    Schacter, D. L. & Tulving, E. Memory Systems (MIT Press, Cambridge, MA, 1994).

    Google Scholar 

  7. 7

    Müller, G. E. & Pilzecker, A. Experimentelle Beitrage zur Lehre vom Gedachtniss. Z. Psychol. 1, 1–288 (1900).

    Google Scholar 

  8. 8

    Duncan, C. P. The retroactive effect of electroshock on learning. J. Comp. Physiol. Psychol. 42, 32–34 (1949).

    CAS  Article  Google Scholar 

  9. 9

    McClelland, J. L., McNaughton, B. L. & O'Reilly, R. C. 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. 102, 419–457 (1995).

    Article  Google Scholar 

  10. 10

    Dudai, Y. The neurobiology of consolidations, or, how stable is the engram? Annu. Rev. Psychol. 55, 51–86 (2004).

    Article  Google Scholar 

  11. 11

    Stickgold, R. Sleep: off-line memory reprocessing. Trends Cogn. Sci. 2, 484–492 (1998).

    CAS  Article  Google Scholar 

  12. 12

    Stickgold, R., Whidbee, D., Schirmer, B., Patel, V. & Hobson, J. A. Visual discrimination task improvement: A multi-step process occurring during sleep. J. Cogn. Neurosci. 12, 246–254 (2000).

    CAS  Article  Google Scholar 

  13. 13

    Stickgold, R., James, L. & Hobson, J. A. Visual discrimination learning requires post-training sleep. Nature Neurosci. 2, 1237–1238 (2000).

    Article  Google Scholar 

  14. 14

    Walker, M., Brakefield, T., Morgan, A., Hobson, J. A. & Stickgold, R. Practice with sleep makes perfect: Sleep dependent motor skill learning. Neuron 35, 205–211 (2002).

    CAS  Article  Google Scholar 

  15. 15

    Fischer, S., Hallschmid, M., Elsner, A. L. & Born, J. Sleep forms memory for finger skills. Proc. Natl Acad. Sci. USA 99, 11987–11991 (2002).

    ADS  CAS  Article  Google Scholar 

  16. 16

    Huber, R., Ghilardi, M. F., Massimini, M. & Tononi, G. Local sleep and learning. Nature 430, 78–81 (2004).

    ADS  CAS  Article  Google Scholar 

  17. 17

    Gais, S., Plihal, W., Wagner, U. & Born, J. Early sleep triggers memory for early visual discrimination skills. Nature Neurosci. 3, 1335–1339 (2000).

    CAS  Article  Google Scholar 

  18. 18

    Walker, M. P. & Stickgold, R. It's practice, with sleep, that makes perfect: Implications of sleep-dependent learning and plasticity for skill performance. Clinics Sports Med. (in the press).

  19. 19

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

    Article  Google Scholar 

  20. 20

    Walker, M. P., Brakefield, T., Hobson, J. A. & Stickgold, R. Dissociable stages of human memory consolidation and reconsolidation. Nature 425, 616–620 (2003).

    ADS  CAS  Article  Google Scholar 

  21. 21

    Ghilardi, M. et al. Patterns of regional brain activation associated with different forms of motor learning. Brain Res. 871, 127–145 (2000).

    CAS  Article  Google Scholar 

  22. 22

    Steriade, M. Active neocortical processes during quiescent sleep. Arch. Ital. Biol. 139, 37–51 (2001).

    CAS  PubMed  Google Scholar 

  23. 23

    Maquet, P. et al. Experience-dependent changes in cerebral activation during human REM sleep. Nature Neurosci. 3, 831–836 (2000).

    CAS  Article  Google Scholar 

  24. 24

    Atienza, M., Cantero, J. L. & Stickgold, R. Posttraining sleep enhances automaticity in perceptual discrimination. J. Cog. Neurosci. 16, 53–64 (2004).

    Article  Google Scholar 

  25. 25

    Roth, D. A., Kishon-Rabin, L., Hildesheimer, M. & Karni, A. A latent consolidation phase in auditory identification learning: Time in the awake state is sufficient. Learn. Mem. 12, 159–164 (2005).

    Article  Google Scholar 

  26. 26

    Robertson, E. M., Pascual-Leone, A. & Press, D. Z. Awareness modifies the skill-learning benefits of sleep. Curr. Biol. 14, 208–212 (2004).

    CAS  Article  Google Scholar 

  27. 27

    Brashers-Krug, T., Shadmehr, R. & Bizzi, E. Consolidation in human motor memory. Nature 382, 252–255 (1996).

    ADS  CAS  Article  Google Scholar 

  28. 28

    American Psychological Association. Diagnostic and Statistical Manual of Mental Disorders, 4th edn (American Psychiatric Association, Washington DC, 1994).

  29. 29

    Manoach, D. S. Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophr. Res. 60, 285–298 (2003).

    Article  Google Scholar 

  30. 30

    Manoach, D. S. et al. A failure of sleep-dependent procedural learning in chronic, medicated schizophrenia. Biol. Psych. 56, 951–956 (2004).

    Article  Google Scholar 

  31. 31

    Ebbinghaus, H. Uber das Gedachtnis (Teachers' College, New York, 1885).

    Google Scholar 

  32. 32

    Smith, C. Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med. Rev. 5, 491–506 (2001).

    CAS  Article  Google Scholar 

  33. 33

    Plihal, W. & Born, J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9, 534–547 (1997).

    CAS  Article  Google Scholar 

  34. 34

    Plihal, W. & Born, J. Memory consolidation in human sleep depends on inhibition of glucocorticoid release. Neuroreport 10, 2741–2747 (1999).

    CAS  Article  Google Scholar 

  35. 35

    Gais, S. & Born, J. Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc. Natl Acad. Sci. USA 101, 2140–2144 (2004).

    ADS  CAS  Article  Google Scholar 

  36. 36

    Schabus, M. et al. Sleep spindles and their significance for declarative memory consolidation. Sleep 27, 1479–1485 (2004).

    Article  Google Scholar 

  37. 37

    Clemens, Z., Fabo, D. & Halasz, P. Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132, 529–535 (2005).

    CAS  Article  Google Scholar 

  38. 38

    Wixted, J. T. The psychology and neuroscience of forgetting. Annu. Rev. Psychol. 55, 235–269 (2004).

    Article  Google Scholar 

  39. 39

    Plihal, W. & Born, J. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology 36, 571–582 (1999).

    CAS  Article  Google Scholar 

  40. 40

    Peigneux, P. et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44, 535–545 (2004).

    CAS  Article  Google Scholar 

  41. 41

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

    CAS  Article  Google Scholar 

  42. 42

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

    ADS  CAS  Article  Google Scholar 

  43. 43

    Smith, C. T., Conway, J. M. & Rose, G. M. Brief paradoxical sleep deprivation impairs reference, but not working, memory in the radial arm maze task. Neurobiol. Learn. Mem. 69, 211–217 (1998).

    CAS  Article  Google Scholar 

  44. 44

    Smith, C. & Rose, G. M. Evidence for a paradoxical sleep window for place learning in the Morris water maze. Physiol. Behav. 59, 93–97 (1996).

    CAS  Article  Google Scholar 

  45. 45

    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).

    CAS  Article  Google Scholar 

  46. 46

    Kuriyama, K., Stickgold, R. & Walker, M. P. Sleep-dependent learning and motor skill complexity. Learn. Mem. 11, 705–713 (2004).

    Article  Google Scholar 

  47. 47

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

    ADS  CAS  Article  Google Scholar 

  48. 48

    Cirelli, C., Gutierrez, C. M. & Tononi, G. Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41, 35–43 (2004).

    CAS  Article  Google Scholar 

  49. 49

    Ribeiro, S., Goyal, V., Mello, C. V. & Pavlides, C. Brain gene expression during REM sleep depends on prior waking experience. Learn. Mem. 6, 500–508 (1999).

    CAS  Article  Google Scholar 

  50. 50

    Ribeiro, S. et al. Induction of hippocampal long-term potentiation during waking leads to increased extrahippocampal zif-268 expression during ensuing rapid-eye-movement sleep. J. Neurosci. 22, 10914–10923 (2002).

    CAS  Article  Google Scholar 

  51. 51

    Frank, M. G., Issa, N. P. & Stryker, M. P. Sleep enhances plasticity in the developing visual cortex. Neuron 30, 275–287 (2001).

    CAS  Article  Google Scholar 

  52. 52

    Shaffery, J. P., Sinton, C. M., Bissette, G., Roffwarg, H. P. & Marks, G. A. Rapid eye movement sleep deprivation modifies expression of long-term potentiation in visual cortex of immature rats. Neuroscience 110, 431–443 (2002).

    CAS  Article  Google Scholar 

  53. 53

    Dave, A. S. & Margoliash, D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290, 812–816 (2000).

    ADS  CAS  Article  Google Scholar 

  54. 54

    Deregnaucourt, S., Mitra, P. P., Feher, O., Pytte, C. & Tchernichovski, O. How sleep affects the developmental learning of bird song. Nature 433, 710–716 (2005).

    ADS  CAS  Article  Google Scholar 

  55. 55

    Schwartz, S., Maquet, P. & Frith, C. Neural correlates of perceptual learning: a functional MRI study of visual texture discrimination. Proc. Natl Acad. Sci. USA 99, 17137–17142 (2002).

    ADS  CAS  Article  Google Scholar 

  56. 56

    Walker, M. P., Stickgold, R., Jolesz, F. A. & Yoo, S. -S. The functional anatomy of sleep-dependent visual skill learning. Cerebral Cortex published online 9 February, 2005 (doi:10.1093/cercor/bhi043).

    Google Scholar 

  57. 57

    Walker, M. P., Stickgold, R., Alsop, D., Gaab, N. & Schlaug, G. Sleep-dependent motor memory plasticity in the human brain. Neuroscience 133, 911–917 (2005).

    CAS  Article  Google Scholar 

  58. 58

    Fosse, M. J., Fosse, R., Hobson, J. A. & Stickgold, R. J. Dreaming and episodic memory: a functional dissociation? J. Cogn. Neurosci. 15, 1–9 (2003).

    Article  Google Scholar 

  59. 59

    Stickgold, R., Malia, A., Maguire, D., Roddenberry, D. & O'Connor, M. Replaying the game: Hypnagogic images in normals and amnesiacs. Science 290, 350–353 (2000).

    ADS  CAS  Article  Google Scholar 

  60. 60

    Maquet, P. Functional neuroimaging of normal human sleep by positron emission tomography. J. Sleep Res. 9, 207–231 (2000).

    CAS  Article  Google Scholar 

  61. 61

    Buzsáki, G. The hippocampo-neocortical dialogue. Cerebral Cortex 6, 81–92 (1996).

    Article  Google Scholar 

  62. 62

    Peigneux, P. et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44, 535–545 (2004).

    CAS  Article  Google Scholar 

  63. 63

    Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A. & Stickgold, R. Practice with sleep makes perfect: sleep dependent motor skill learning. Neuron 35, 205–211 (2002).

    CAS  Article  Google Scholar 

  64. 64

    Datta, S. Avoidance task training potentiates phasic pontine-wave density in the rat: A mechanism for sleep-dependent plasticity. J. Neurosci. 20, 8607–8613 (2000).

    CAS  Article  Google Scholar 

  65. 65

    Gais, S., Molle, M., Helms, K. & Born, J. Learning-dependent increases in sleep spindle density. J. Neurosci. 22, 6830–6834 (2002).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the US National Institutes of Health.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Robert Stickgold.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Additional information

Author Information Reprints and permissions information is available at npg.nature.com/reprintsandpermissions.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stickgold, R. Sleep-dependent memory consolidation. Nature 437, 1272–1278 (2005). https://doi.org/10.1038/nature04286

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

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