Does sleep promote motor learning? Implications for physical rehabilitation

Physical Therapy

Volumn 89, Issue 4, 2009, Pages 370-383

  Siengsukon, Catherine F ^a   Boyd, Lara A ^b  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EPISODIC MEMORY; HUMAN; LEARNING; LONG TERM POTENTIATION; MEMORY; MOTOR PERFORMANCE; NEUROIMAGING; PHYSIOTHERAPY; REM SLEEP; REVIEW; SEMANTIC MEMORY; SLEEP; STROKE; ADULT; AGING; CHRONIC DISEASE; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; REFERENCE VALUE; SLEEP STAGE; TASK PERFORMANCE;

ADULT; AGING; CHRONIC DISEASE; HUMANS; LEARNING; MEMORY; MIDDLE AGED; MOTOR SKILLS; PHYSICAL THERAPY MODALITIES; PSYCHOMOTOR PERFORMANCE; REFERENCE VALUES; SLEEP; SLEEP STAGES; STROKE; TASK PERFORMANCE AND ANALYSIS; YOUNG ADULT;

EID: 64749095796     PISSN: 00319023     EISSN: None     Source Type: Journal    
DOI: 10.2522/ptj.20080310     Document Type: Review

References (125)

1. Rosamond W, Flegal K, Furie K, étal. Heart disease and stroke statistics- 2008 update: a report from the Ameri- can Heart Association Statistics Com- mittee and Stroke Statistics Sub- committee. Circulation. 2008;117: e25-el46.
2. Wade DT, Langton-Hewer R, Wood VA, et al. The hémiplégie arm after stroke: measurement and recovery. Neurol Neurosurg Psychiatry. 1983;46:521- 524.
3. Broeks JG, Lankhorst GJ, Rumping K, Prevo AJ. The long-term outcome of arm function after stroke: results of a follow-up study. Disabil Rehabil. 1999; 21:357-364.
4. Walker MP, Stickgold R. Sleep, memory, and plasticity. Annu Rev Psychol. 2006; 57:139-166.
5. Walker MP, Stickgold R. Sleep-dependent learning and memory consolidation. Neu- ron. 2004;44:121-133.
6. Rauchs G, Desgranges B, Foret J, Eu- stache F. The relationships between memory systems and sleep stages. J Sleep Res. 2005;14:123-140.
7. Peigneux P, Laureys S, Delbeuck X, Ma- quet P. Sleeping brain, learning brain: the role of sleep for memory systems. Neu- roreport. 2001;12:A111-A124.
8. Stickgold R, Walker MP. Sleep and mem- ory: the ongoing debate. Sleep. 2005; 28:1225-1227.
9. Stickgold R. Sleep-dependent memory consolidation. Nature. 2005:437(7063): 1272-1278.
10. Stickgold R, Walker MP. Memory consol- idation and reconsolidation: what is the role of sleep? Trends Neurosci. 2005; 28:408-415.
11. McGaugh JL. Memory: a century of consolidation. Science. 2000;287(5451): 248-251.
12. 12 Robertson EM, Pascual-Leone A, Miall RC. Current concepts in procedural con- solidation. Nat Rev Neurosci. 2004; 5:576-582.
13. Vertes RP. Memory consolidation in sleep; dream or reality. Neuron. 2004; 44:135-148.
14. Siegel JM. The REM sleep-memory con- solidation hypothesis. Science. 2001; 294(5544):1058-1063.
15. Vertes RP, Siegel JM. Time for the sleep community to take a critical look at the purported role of sleep in memory pro- cessing. Sleep. 2005;28:1228-1229; dis- cussion I23O-I223.
16. Keisler A, Ashe J, Willingham DT. Time of day accounts for overnight improve- ment in sequence learning. Learn Mem. 2007;14:669-672.
17. Rickard TC, Cai DJ, Rieth CA, et al. Sleep does not enhance motor sequence learn- ing. / Exp Psychol Learn Mem Cogn. 2008;34:834-842.
18. Korman M, Raz N, Flash T, Kami A. Multiple shifts in the representation of a mo- tor sequence during the acquisition of skilled performance. Proc Natl Acad Sci USA. 2003;100:12492-12497.
19. Walker MP, Brakefield T, Morgan A, et al. Practice with sleep makes perfect: sleep- dependent motor skill learning. Neuron. 2002;35:205-211.
20. Walker MP, Brakefield T, Seidman J, et al. Sleep and the time course of motor skill learning. Learn Mem. 2003;10:275-284.
21. Walker MP, Brakefield T, Hobson JA, Stickgold R. Dissociable stages of human memory consolidation and reconsolida- tion. Nature. 2003;425(6958):6l6- 620.
22. Fischer S, Hallschmid M, Eisner AL, Born J. Sleep forms memory for finger skills. Proc Natl Acad Sci USA. 2002;99: 11987-11991.
23. Nishida M, Walker MP. Daytime naps, motor memory consolidation and region- ally specific sleep spindles. PLoS ONE. 2007;2:e341.
24. Backhaus J, Junghanns K. Daytime naps improve procedural motor memory. Sleep Med. 2006;7:508-512.
25. Spencer RM, Gouw AM, Ivry RB. Age- related decline of sleep-dependent con- solidation. Learn Mem. 2007; 14: 480-484.
26. Backhaus J, Born J, Hoeckesfeld R, et al. Midlife decline in declarative memory consolidation is correlated with a decline in slow wave sleep. Learn Mem. 2007;14:336-341.
27. Siengsukon CF, Boyd LA. Sleep to learn after stroke: implicit and explicit off-line motor learning. Neurosci Lett. 2009;451:1-5.
28. Danker-Hopfe H, Schafer M, Dorn H, et al. Percentile reference charts for se- lected sleep parameters for 20- to 80- year-old healthy subjects from the SIESTA database. Somnolgie. 2005;9:3-14.
29. Buckley TM, Schatzberg AF. Aging and the role of the HPA axis and rhythm in sleep and memory-consolidation. Am J Geriatr Psychiatry. 2005;13:344-352.
30. Crowley K, Trinder J, Kim Y, et al. The effects of normal aging on sleep spindle and K-complex production. Clin Neuro- physiol. 2002;113:1615-1622.
31. Nicolas A, Petit D, Rompre S, Montplaisir J. Sleep spindle characteristics in healthy subjects of different age groups. Clin Neurophysiol. 2001;112:521-527.
32. Gomez Beldarrain M, Astorgano AG, Gonzalez AB, Garcia-Monco JC. Sleep im- proves sequential motor learning and performance in patients with prefrontal lobe lesions. Clin Neurol Neurosurg. 2008;110:245-252.
33. Siengsukon CF, Boyd LA. Sleep enhances implicit motor skill learning in individu- als poststroke. Top Stroke Rehabil. 2008;15:1-12.
34. Vock J, Achermann P, Bischof M, et al. Evolution of sleep and sleep EEG after hemispheric stroke. J Sleep Res. 2002;11: 331-338.
35. Gottselig JM, Bassetti CL, Achermann P. Power and coherence of sleep spindle frequency activity following hemispheric stroke. Brain. 2002;125(pt 2):373-383.
36. Rechtschaffen A, Siegel J. Sleep and dreaming. In: Kandel ER, Schwartz JH, Jessell TM, eds. Principles of Neural Sci- ence. 4th ed. New York, NY: McGraw- Hill; 2000:936-947.
37. Huether SE, McCance KL. Understand- ing Pathophysiology. 3rd ed. St Louis, MO: CV Mosby Inc; 2004.
38. De Gennaro L, Ferrara M. Sleep spindles: an overview. Sleep Med Rev. 2003:7: 423-440.
39. Jankel WR, Niedermeyer E. Sleep spin- dles/ Clin Neurophysiol. 1985;2:1-35.
40. Leppavuori A, Pohjasvaara T, Vataja R, et al. Insomnia in ischemic stroke pa- tients. Cerebrovasc Dis. 2002;14:90-97.
41. Bassetti CL. Sleep and stroke. Semin Neu- rol. 2005;25:19-32.
42. Bassetti CL, Aldrich MS. Sleep electroen- cephalogram changes in acute hemi- spheric stroke. Sleep Med. 2001;2: 185-194.
43. Müller C, Achermann P, Bischof M, et al. Visual and spectral analysis of sleep EEG in acute hemispheric stroke. Eur Neurol. 2002;48:164-171.
44. Giubilei F, Iannilli M, Vitale A, et al. Sleep patterns in acute ischemic stroke. Acta Neurol Scand. 1992;86:567-571.
45. Kandel ER, Kupfermann I, Iversen S. Learning and memory. In: Kandel ER, Schwartz JH, Jessell TM, eds. Principles of Neural Science. 4th ed. New York, NY: McGraw-Hill; 2000:1227-1246.
46. Walker MP. A refined model of sleep and the time course of memory formation. Behav Brain Sci. 2005;28:51-64; discus- sion 64-104.
47. Alberini CM. Mechanisms of memory sta- bilization: are consolidation and recon- solidation similar or distinct processes? Trends Neurosci. 2005;28:51-56.
48. Stickgold R, Walker MP. Sleep-dependent memory consolidation and reconsolida- tion. Sleep Med. 2007;8:331-343.
49. Squire LR. Mechanisms of memory. Sci- ence. 1986;232(4758):1612-1619.
50. Squire LR. Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem. 2004;82: 171-177.
51. Squire LR, Stark CE, Clark RE. The medial temporal lobe. Annu Rev Neurosci. 2004;27:279-306.
52. Squire LR, Zola SM. Structure and func- tion of declarative and nondeclarative memory systems. Proc Natl Acad Sci USA. 1996;93:13515-13522.
53. Doyon J, Penhune V, Ungerleider LG. Distinct contribution of the cortico- striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia. 2003;41:252-262.
54. Hikosaka O, Nakamura K, Sakai K, Naka- hara H. Central mechanisms of motor skill learning. Curr Opin Neurobiol. 2002;12:217-222.
55. Hikosaka O, Nakahara H, Rand MK, et al. Parallel neural networks for learning se- quential procedures. Trends Neurosci. 1999;22:464-471.
56. Stickgold R, Whidbee D, Schirmer B, et al. Visual discrimination task improve- ment: A multi-step process occurring during sleep. / Cogn Neurosci. 2000;12: 246-254.
57. Gais S, Plihal W, Wagner U, Born J. Early sleep triggers memory for early visual dis- crimination skills. Nat Neurosci. 2000; 3:1335-1339.
58. Giuditta A, Ambrosini MV, Montagnese P, et al. The sequential hypothesis of the function of sleep. Behav Brain Res. 1995;69:157-166.
59. Plihal WB, Born J. Effects of early and late noctural sleep on declarative and procedural memory. J Cogn Neurosci. 1997;9: 534-547.
60. Plihal WB, Pietrowsky R, Born J. Dexa- methasone blocks sleep induced im- provement of declarative memory. Psy- choneuroendocrinology. 1999;24:313-331.
61. De Koninck J, Lorrain D, Christ G, et al. Intensive language learning and in- creases in rapid eye movement sleep: ev- idence of a performance factor. IntJPsy- chophysiol. 1989;8:43-47.
62. Wagner U, Gais S, Born J. Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn Mem. 2001;8:112-119.
63. Smith C. Sleep states and memory processes. Behav Brain Res. 1995;69: 137-145.
64. Smith C, MacNeill C. Impaired motor memory for a pursuit rotor task following Stage 2 sleep loss in college students. / Sleep Res. 1994;3:206-213
65. Kami A, Tanne D, Rubenstein BS, et al. Dependence on REM sleep of overnight improvement of a perceptual skill. Sci- ence. 1994;265(5172):679-682.
66. Fogel SM, Smith CT, Cote KA. Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems. Behav Brain Res. 2007;180:48-61.
67. Peters KR, Smith V, Smith CT. Changes in sleep architecture following motor learn- ing depend on initial skill level. / Cogn Neurosci. 2007;19:817-829.
68. Willingham DB, Goedert-Eschmann K. The relation between implicit and explicit learning: Evidence for parallel de- velopment. Psychological Science. 1999;10:531-534.
69. Boyd LA, Winstein CJ. Impact of explicit information on implicit motor-sequence learning following middle cerebral artery stroke. Phys Ther. 2003;83:976-989.
70. Boyd LA, Winstein CJ. Providing explicit information disrupts implicit motor learning after basal ganglia stroke. Learn Mem. 2004;11:388-396.
71. Shea CH, WuIfG, Whitacre CA, Park JH. Surfing the implicit wave. Q J Exp Psy- chol A. 2001;54:841-862.
72. Green TD, Flowers JH. Comparison of implicit and explicit learning processes in a probabilistic task. Percept Mot Skills. 2003;97:299-314.
73. Green TD, Flowers JH. Implicit versus explicit learning processes in a probabi- listic, continuous fine-motor catching task. / Mot Behav. 1991;23:293-300.
74. Magill RA. 1997 C. H. McCloy Research Lecture: Knowledge is more than we can talk about: implicit learning in motor skill acquisition. Res Q Exerc Sport. 1998; 69:104-110.
75. Reber AS, Kassin SM, Lewis S, Cantor G. On the relationship between implicit and explicit modes in the learning of a com- plex rule structure. / Exp Psychol Hum Learn Mem. 1980;6:492-502.
76. Boyd LA, Quaney BM, Pohl PS, Winstein CJ. Learning implicitly: effects of task and severity after stroke. Neurorehabil Neu- ral Repair. 2007;21:444-454.
77. Robertson EM, Pascual-Leone A, Press DZ. Awareness modifies the skill-learning benefits of sleep. Curr Biol. 2004; 14:208-212.
78. Fischer S, Drosopoulos S, Tsen J, Bom J. Implicit learning: explicit knowing: a role for sleep in memory system interac- tion./ Cogn Neurosci. 2006;18:311-319.
79. Drosopoulos S, Wagner U, Bom J. Sleep enhances explicit recollection in recognition memory. Learn Mem. 2005; 12: 44-51.
80. Spencer RM, Sunm M, Ivry RB. Sleep- dependent consolidation of contextual learning. Curr Biol. 2006;16:1001-1005.
81. Wagner U, Gais S, Haider H, et al. Sleep inspires insight. Nature. 2004; 427(6972):352-355.
82. Bom J, Wagner U. Awareness in memory: being explicit about the role of sleep. Trends Cogn Sci. 2004;8:242-244.
83. Poldrack RA, Packard MG. Competition among multiple memory systems: con- verging evidence from animal and hu- man brain studies. Neuropsychologia. 2003;41:245-251.
84. Cohen DA, Pascual-Leone A, Press DZ, Robertson EM. Off-line learning of motor skill memory: a double dissociation of goal and movement. Proc Natl Acad Sci USA. 2005;102:18237-18241.
85. Robertson EM, Cohen DA. Understanding consolidation through the architecture of memories. Neuroscientist. 2006; 12:261-271.
86. Schmidt RA, Lee TD. Motor Control and Learning: A Behavioral Emphasis. 3rd ed. Champaign, IL: Human Kinetics Inc; 1999.
87. Walker MP, Stickgold R, Alsop D, et al. Sleep-dependent motor memory plastic- ity in the human brain. Neuroscience. 2005;133:911-917.
88. Maquet P, Schwartz S, Passingham R, Frith C. Sleep-related consolidation of a visuomotor skill: brain mechanisms as as- sessed by functional magnetic resonance imaging. / Neurosci. 2003:23: 1432-1440.
89. Pew RW. Levels of analysis in motor con- trol. Brain Res. 1974;71:393-400.
90. Wulf G, Schmidt RA. Variability of prac- tice and implicit motor learning. / Exp Psychol Learn Mem Cogn. 1997;23: 987-1006.
91. Boyd LA, Winstein CJ. Explicit informa- tion interferes with implicit motor learn- ing of both continuous and discrete movement tasks after stroke. / Neurol Phys Ther. 2006:30:46-57.
92. Boyd LA, Winstein CJ. Cerebellar stroke impairs temporal but not spatial accuracy during implicit motor learning. Neurore- habil Neural Repair. 2004;18:134-143.
93. Song S, Howard JH Jr, Howard DV. Sleep does not benefit probabilistic motor sequence learning. Neurosci. 20O7;27: 12475-12483.
94. WuIfG, Shea CH. Principles derived from the study of simple skills do not generalize to complex skill learning. Psychon Bull Rev. 2002;9:185-211.
95. Kuriyama K, Stickgold R, Walker MP. Sleep-dependent learning and motor-skill complexity. Learn Mem. 2004;11: 705-713.
96. Maquet P, Laureys S, Peigneux P, et al. Experience-dependent changes in cerebral activation during human REM sleep. Nat Neurosci. 200O;3:831-836.
97. Peigneux P, Laureys S, Fuchs S, et al. Learned material content and acquisition level modulate cerebral reactivation dur- ing posttraining rapid-eye-movements sleep. Neurolmage. 2003;20:125-134.
98. Laureys S, Peigneux P, Phillips C, et al. Experience-dependent changes in cere- bral functional connectivity during hu- man rapid eye movement sleep. Neuro- science. 2001;105:521-525.
99. Fischer S, Nitschke MF, Melchert UH, et al. Motor memory consolidation in sleep shapes more effective neuronal representations. / Neurosci. 2005;25: 11248-11255.
100. Dang-Vu TT, Desseilles M, Peigneux P, Maquet P. A role for sleep in brain plasticity. Pediatr Rehabil. 2006;9:98-118.
101. Benington JH, Frank MG. Cellular and molecular connections between sleep and synaptic plasticity. Prog Neurobiol. 2003;69:71-101.
102. Graves L, Pack A, Abel T. Sleep and memory: a molecular perspective. Trends Neurosci. 2001;24:237-243.
103. Fogel SM, Smith CT. Learning-dependent changes in sleep spindles and Stage 2 sleep./Sleep Res. 2006;15:250-255.
104. Ribeiro S, Nicolelis MA. Reverberation, storage, and postsynaptic propagation of memories during sleep. Learn Mem. 2004;11:686-696.
105. Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev. 2006;10:49-62.
106. Frank MG, Benington JH. The role of sleep in memory consolidation and brain plasticity: dream or reality? Neuroscien- tist. 2006;12:477-488.
107. Siengsukon CF, Boyd LA. Sleep enhances off-line spatial and temporal motor learn- ing after stroke. Neurorehabil Neural Repair. In press.
108. Schredl M, Weber B, Leins ML, Heuser I. Donepezil-induced REM sleep augmenta- tion enhances memory performance in elderly, healthy persons. Exp Gerontol. 2001;36:353-361.
109. Pohl PS, McDowd JM, Filion DL, et al. Implicit learning of a perceptual-motor skill after stroke. Phys Ther. 2001;81: 1780-1789.
110. Winstein CJ, Merians AS, Sullivan KJ. Mo- tor learning after unilateral brain damage. Neuropsychologia. 1999;37:975-987.
111. Platz T, Denzler P, Kaden B, Mauritz KH. Motor learning after recovery from hemi- paresis. Neuropsychologia. 1994;32: 1209-1223.
112. Hanion RE. Motor learning following uni- lateral stroke. Arch Phys Med Rehabil. 1996;77:811-815.
113. 113 Pohl PS, McDowd JM, Filion D, et al. Implicit learning of a motor skill after mild and moderate stroke. Clin Rehabil. 2006;20:246-253.
114. Shimizu T, Hosaki A, Hino T, et al. Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain. 2002;125(pt 8): 1896-1907.
115. Liepert J, Hamzei F, Weiller C. Motor cor- tex disinhibition of the unaffected hemi- sphere after acute stroke. Muscle Nerve. 2000;23:1761-1763.
116. Traversa R, Cicinelli P, Pasqualetti P, et al. Follow-up of interhemispheric dif- ferences of motor evoked potentials from the "affected" and "unaffected" hemispheres in human stroke. Brain Res. 1998;803:1-8.
117. Cicinelli P, Traversa R, Rossini PM. Post-stroke reorganization of brain motor output to the hand: a 2-4 month follow-up with focal magnetic transcranial stimula- tion. Electroencephalogr Clin Neuro- physiol. 1997;105:438-450.
118. Sawaki L, Butler AJ, Xiaoyan L, et al. Constraint-induced movement therapy results in increased motor map area in subjects 3 to 9 months after stroke. Neu- rorehabil Neural Repair. 2008;22: 505-513.
119. 119 Liepert J, Bauder H, Wolfgang HR, et al. Treatment-induced cortical reorganiza- tion after stroke in humans. Stroke. 2000;31:1210-1216.
120. Catano A, Houa M, Caroyer JM, et al. Magnetic transcranial stimulation in acute stroke: early excitation threshold and functional prognosis. Electroen- cephalogr Clin Neurophysiol. 1996,101: 233-239.
121. Traversa R, Cicinelli P, Oliveri M, et al. Neurophysiological follow-up of motor cortical output in stroke patients. Clin Neurophysiol. 2000;111:1695-1703.
122. Koski L, Memar TJ, Dobkin BH. Immediate and long-term changes in corticomotor output in response to rehabilitation: correlation with functional improve- ments in chronic stroke. Neurorehabil Neural Repair. 2004;18:230-249.
123. Rossini PM, Pauri F. Neuromagnetic inte- grated methods tracking human brain mechanisms of sensorimotor areas "plas- tic" reorganisation. Brain Res Brain Res Rev. 2000;33:131-154.
124. Talelli P, Greenwood RJ, Rothwell JC. Arm function after stroke: neurophysiological correlates and recovery mechanisms assessed by transcranial magnetic stimulation. Clin Neurophysiol. 2006; 117:1641-1659.
125. 125 Liepert J, RestemeyerC, KucinskiT, et al. Motor strokes: the lesion location determines motor excitability changes. Stroke. 2005;36:2648-2653.