Sleep-dependent memory consolidation

Nature

Volumn 437, Issue 7063, 2005, Pages 1272-1278

  Stickgold, Robert ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; MOLECULAR BIOLOGY; PROBLEM SOLVING; SIGNAL ENCODING;

MEMORY ENCODING; PHENOMENOLOGY; SLEEP-DEPENDENT MEMORY CONSOLIDATIONS;

SLEEP RESEARCH;

SLEEP;

ADAPTATION; COGNITIVE DEFECT; DREAM; ELECTROENCEPHALOGRAM; EMOTIONAL STRESS; EVENT RELATED POTENTIAL; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; LEARNING; MEMORY; MEMORY CONSOLIDATION; MENTAL DISEASE; NEUROPHYSIOLOGY; NONHUMAN; PLASTICITY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REM SLEEP; REM SLEEP DEPRIVATION; REVIEW; SLEEP; SLEEP STAGE; SLOW WAVE SLEEP; TASK PERFORMANCE; VISUAL DISCRIMINATION;

EID: 27644573483     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature04286     Document Type: Review

References (65)

1. Institutes of Oratory. Quintilian 〈http://lee.engl.iastate.edu/11/ chapter2.html〉 (2004).
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).
3. Stickgold, R. & Walker, M. P. Sleep and memory: the ongoing debate. Sleep 28, 1225-1227 (2005).
4. Walker, M. P. & Stickgold, R. Sleep-dependent learning and memory consolidation. Neuron 44, 121-133 (2004).
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).
6. Schacter, D. L. & Tulving, E. Memory Systems (MIT Press, Cambridge, MA, 1994).
7. Müller, G. E. & Pilzecker, A. Experimentelle Beitrage zur Lehre vom Gedachtniss. Z. Psychol. 1, 1-288 (1900).
8. Duncan, C. P. The retroactive effect of electroshock on learning. J. Comp. Physiol. Psychol. 42, 32-34 (1949).
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).
10. Dudai, Y. The neurobiology of consolidations, or, how stable is the engram? Annu. Rev. Psychol. 55, 51-86 (2004).
11. Stickgold, R. Sleep: off-line memory reprocessing. Trends Cogn. Sci. 2, 484-492 (1998).
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).
13. Stickgold, R., James, L. & Hobson, J. A. Visual discrimination learning requires post-training sleep. Nature Neurosci. 2, 1237-1238 (2000).
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).
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).
16. Huber, R., Ghilardi, M. F., Massimini, M. & Tononi, G. Local sleep and learning. Nature 430, 78-81 (2004).
17. Gais, S., Plihal, W., Wagner, U. & Born, J. Early sleep triggers memory for early visual discrimination skills. Nature Neurosci. 3, 1335-1339 (2000).
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. Walker, M. P. et al. Sleep and the time course of motor skill learning. Learn. Mem. 10, 275-284 (2003).
20. Walker, M. P., Brakefield, T., Hobson, J. A. & Stickgold, R. Dissociable stages of human memory consolidation and reconsolidation. Nature 425, 616-620 (2003).
21. Ghilardi, M. et al. Patterns of regional brain activation associated with different forms of motor learning. Brain Res. 871, 127-145 (2000).
22. Steriade, M. Active neocortical processes during quiescent sleep. Arch. Ital. Biol. 139, 37-51 (2001).
23. Maquet, P. et al. Experience-dependent changes in cerebral activation during human REM sleep. Nature Neurosci. 3, 831-836 (2000).
24. Atienza, M., Cantero, J. L. & Stickgold, R. Posttraining sleep enhances automaticity in perceptual discrimination. J. Cog. Neurosci. 16, 53-64 (2004).
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).
26. Robertson, E. M., Pascual-Leone, A. & Press, D. Z. Awareness modifies the skill-learning benefits of sleep. Curr. Biol. 14, 208-212 (2004).
27. Brashers-Krug, T., Shadmehr, R. & Bizzi, E. Consolidation in human motor memory. Nature 382, 252-255 (1996).
28. American Psychological Association. Diagnostic and Statistical Manual of Mental Disorders, 4th edn (American Psychiatric Association, Washington DC, 1994).
29. Manoach, D. S. Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophr. Res. 60, 285-298 (2003).
30. Manoach, D. S. et al. A failure of sleep-dependent procedural learning in chronic, medicated schizophrenia. Biol. Psych. 56, 951-956 (2004).
31. Ebbinghaus, H. Uber das Gedachtnis (Teachers' College, New York, 1885).
32. Smith, C. Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med. Rev. 5, 491-506 (2001).
33. Plihal, W. & Born, J. Effects of early and late nocturnal sleep on declarative and procedural memory. J. Cogn. Neurosci. 9, 534-547 (1997).
34. Plihal, W. & Born, J. Memory consolidation in human sleep depends on inhibition of glucocorticoid release. Neuroreport 10, 2741-2747 (1999).
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).
36. Schabus, M. et al. Sleep spindles and their significance for declarative memory consolidation. Sleep 27, 1479-1485 (2004).
37. Clemens, Z., Fabo, D. & Halasz, P. Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 132, 529-535 (2005).
38. Wixted, J. T. The psychology and neuroscience of forgetting. Annu. Rev. Psychol. 55, 235-269 (2004).
39. Plihal, W. & Born, J. Effects of early and late nocturnal sleep on priming and spatial memory. Psychophysiology 36, 571-582 (1999).
40. Peigneux, P. et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44, 535-545 (2004).
41. Louie, K. & Wilson, M. A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29, 145-156 (2001).
42. Wilson, M. A. & McNaughton, B. L. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676-679 (1994).
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).
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).
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).
46. Kuriyama, K., Stickgold, R. & Walker, M. P. Sleep-dependent learning and motor skill complexity. Learn. Mem. 11, 705-713 (2004).
47. Wagner, U., Gais, S., Haider, H., Verleger, R. & Born, J. Sleep inspires insight. Nature 427, 352-355 (2004).
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).
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).
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).
51. Frank, M. G., Issa, N. P. & Stryker, M. P. Sleep enhances plasticity in the developing visual cortex. Neuron 30, 275-287 (2001).
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).
53. Dave, A. S. & Margoliash, D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290, 812-816 (2000).
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).
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).
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).
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).
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).
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).
60. Maquet, P. Functional neuroimaging of normal human sleep by positron emission tomography. J. Sleep Res. 9, 207-231 (2000).
61. Buzsáki, G. The hippocampo-neocortical dialogue. Cerebral Cortex 6, 81-92 (1996).
62. Peigneux, P. et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44, 535-545 (2004).
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).
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).
65. Gais, S., Molle, M., Helms, K. & Born, J. Learning-dependent increases in sleep spindle density. J. Neurosci. 22, 6830-6834 (2002).