The effect of sleep on motor learning in the aging and stroke population - A systematic review

Restorative Neurology and Neuroscience

Volumn 34, Issue 1, 2015, Pages 153-164

  Backhaus, W ^a   Kempe, S ^a   Hummel, F C ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

aging; consolidation; motor memory; Sleep; stroke; systematic review

Indexed keywords

AGING; BODY MOVEMENT; CEREBROVASCULAR ACCIDENT; HAND MOVEMENT; HUMAN; LEARNING; MEMORY CONSOLIDATION; MOTOR PERFORMANCE; PRIORITY JOURNAL; REVIEW; SLEEP; SYSTEMATIC REVIEW; TASK PERFORMANCE; WAKEFULNESS; MEMORY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; PSYCHOMOTOR PERFORMANCE;

AGING; HUMANS; LEARNING; MEMORY; PSYCHOMOTOR PERFORMANCE; SLEEP; STROKE;

EID: 84956817436     PISSN: 09226028     EISSN: 18783627     Source Type: Journal    
DOI: 10.3233/RNN-150521     Document Type: Review

References (63)

1. Al-Sharman, A., & Siengsukon, C. F. (2013). Sleep enhances learning of a functional motor task in young adults. Phys Ther, 93, 1625-1635.
2. Al-Sharman, A., & Siengsukon, C. F. (2014). Performance on a functional motor task is enhanced by sleep in middle-aged and older adults. J Neurol Phys Ther, 38, 161-169.
3. Al-Sharman, A., &Siengsukon, C. F. (2014). Time rather than sleep appears to enhance off-line learning and transfer of learning of an implicit continuous task. Nat Sci Sleep, 6, 27-36.
4. Born, J., Rasch, B., & Gais, S. (2006). Sleep to remember. Neuroscientist, 12, 410-424.
5. Born, J., & Wilhelm, I. (2012). System consolidation of memory during sleep. Psychol Res, 76, 192-203.
6. Boyd, L. A., Vidoni, E. D., & Siengsukon, C. F. (2008) Multidimensional motor sequence learning is impaired in older but not younger or middle-aged adults. Phys Ther, 88, 351-362.
7. Brown, R. M., Robertson, E. M., &Press, D. Z. (2009). Sequence skill acquisition and off-line learning in normal aging. PLoS One, 4, e6683.
8. Cajochen, C., Münch, M., Knoblauch, V., Blatter, K., & Wirz-Justice, A. (2006). Age-related changes in the circadian and homeostatic regulation of human sleep. Chronobiol Int, 23, 461-474.
9. Campos, T. F., Diógenes, F. P., França, F. R., Dantas, R. C., Araujo, J. F., & Menezes, A., A. L. (2005). The sleep-wake cycle in the late stage of cerebral vascular accident recovery. Biol Rhythm Res, 36, 109-114.
10. Campos, T. F., Tostes, M., Barroso, M., Braga, A., Silveira, G., Protasio, L., Melo, D., Amália, A., Souza, T., Dantas, G., & Araujo, J. F. (2013) Sleep disturbances complaints in stroke: Implications for sleep medicine. 55, 98-102.
11. Dayanidhi, S., & Valero-Cuevas, F. J. (2014). Dexterous manipulation is poorer at older ages and is dissociated from decline of hand strength. J Gerontol A Biol Sci Med Sci, 69, 1-7.
12. DGSM, Deutsche Gesellschaft für Schlafmedizin, Schulz, H., Geisler, P., & Rodenbeck, A. (1997) Kompendium der Schlafmedizin für Ausbildung, Klinik und Praxis. ecomed, Landsberg am Lech.
13. Dhand, R., & Sohal, H. (2006). Good sleep, bad sleep! The role of daytime naps in healthy adults. Curr Opin Pulm Med, 12, 379-382.
14. Djonlagic, I., Guo, M., Matteis, P., Carusona, A., Stickgold, R., & Malhotra, A. (2014). Untreated sleep-disordered breathing: Links to aging-related decline in sleep-dependent memory consolidation. PLoS One, 9, 1-7.
15. Doyon, J., Korman, M., Morin, A., Dostie, V., Hadj Tahar, A., Benali, H., Karni, A., Ungerleider, L. G., & Carrier, J. (2009). Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning. Exp Brain Res, 195, 15-26.
16. Eggert, T., Dorn, H., Sauter, C., Nitsche, M. A., Bajbouj, M., & Danker-Hopfe, H. (2013). No effects of slow oscillatory transcranial direct current stimulation (tDCS) on sleep-dependent memory consolidation in healthy elderly subjects. Brain Stimul, 6, 938-945.
17. Fischer, S., & Born, J. (2009). Anticipated reward enhances offline learning during sleep. J Exp Psychol Learn Mem Cogn, 35, 1586-1593.
18. Fogel, S., Martin, N., Lafortune, M., Barakat, M., Debas, K., Laventure, S., Latreille, V., Gagnon, J.-F., Doyon, J., & Carrier, J. (2012). NREM sleep oscillations and brain plasticity in aging. Front Neurol, 3, 176.
19. Fogel, S. M., Albouy, G., Vien, C., Popovicci, R., King, B. R., Hoge, R., Jbabdi, S., Benali, H., Karni, A., Maquet, P., Carrier, J., & Doyon, J. (2014). fMRI and sleep correlates of the age-related impairment in motor memory consolidation. Hum Brain Mapp, 35, 3625-3645.
20. Foley, D. J., Monjan, A. A., Brown, S. L., Simonsick, E. M., Wallace, R. B., & Blazer, D. G. (1995). Sleep complaints among elderly persons: An epidemiologic study of three communities. Sleep, 18, 425-432.
21. Foley, D. J., Vitiello, M. V., Bliwise, D. L., Ancoli-Israel, S., Monjan, A. A., &Walsh, J. K. (2007). Frequent napping is associated with excessive daytime sleepiness, depression, pain, and nocturia in older adults: Findings from the National Sleep Foundation "2003 Sleep in America". Poll Am J Geriatr Psychiatry, 15, 344-350.
22. Genzel, L., Kiefer, T., Renner, L., Wehrle, R., Kluge, M., Grözinger, M., Steiger, A., & Dresler, M. (2012). Sex and modulatory menstrual cycle effects on sleep related memory consolidation. Psychoneuroendocrinology, 37, 987-998.
23. Gomez Beldarrain, M., Astorgano, A. G., Gonzalez, A. A. B., Garcia-Monco, J. C., Beldarrain, M. G., Gomez, M., & Bilbao, A. (2008). Sleep improves sequential motor learning and performance in patients with prefrontal lobe lesions. Clin Neurol Neurosurg, 110, 245-252.
24. Gottselig, J. M., Bassetti, C. L., & Achermann, P. (2002). Power and coherence of sleep spindle frequency activity following hemispheric stroke. Brain, 125, 373-383.
25. Gudberg, C., Wulff, K., & Johansen-Berg, H. (2015). Sleepdependent motor memory consolidation in older adults depends on task demands. Neurobiol Aging, 36, 1409-1416.
26. Hayashi, M., Masuda, A., & Hori, T. (2003). The alerting effects of caffeine, bright light and face washing after a short daytime nap. Clin Neurophysiol, 114, 2268-2278.
27. Heise, K-F, Zimerman, M., Hoppe, J., Gerloff, C., Wegscheider, K., & Hummel, F. C. (2013). The aging motor system as a model for plastic changes of GABA-mediated intracortical inhibition and their behavioral relevance. J Neurosci, 33, 9039-9049.
28. Holland, P., & Lewis, P. A. (2007). Emotional memory: Selective enhancement by sleep. Curr Biol, 17, R179-R181.
29. Hornung, O. P., Danker-Hopfe, H., & Heuser, I. (2005). Age-related changes in sleep and memory: Commonalities and interrelationships. Exp Gerontol, 40, 279-285.
30. Hu, P., Stylos-Allan, M., & Walker, M. P. (2006). Sleep facilitates consolidation of emotional declarative memory. Psychol Sci, 17, 891-898.
31. Iber, C., Ancoli-Israel, S., & Chesson A. Q. S. (2007) The AASM manual for the scoring of sleep and associated events: Rules, terminology, and technical specifications. American Academy of Sleep Medicine, Westchester, IL, USA.
32. King, B. R., Fogel, S. M., Albouy, G., & Doyon, J. (2013). Neural correlates of the age-related changes in motor sequence learning and motor adaptation in older adults. Front Hum Neurosci, 7, 142.
33. Leng, Y., Cappuccio, F. P., Wainwright, N. W. J., Surtees, P. G., Luben, R., Brayne, C., & Khaw, K.-T. (2015) Sleep duration and risk of fatal and nonfatal stroke: A prospective study and metaanalysis. Neurology, [epub ahead of print].
34. Marshall, L., Helgadóttir, H., Mölle, M., &Born, J. (2006). Boosting slowoscillations during sleep potentiates memory. Nature, 444, 610-613.
35. Nemeth, D., Janacsek, K., Londe, Z., Ullman, M. T., Howard, D. V., & Howard, J. H. (2010). Sleep has no critical role in implicit motor sequence learning in young and old adults. Exp Brain Res, 201, 351-358.
36. Nishida, M., & Walker, M. P. (2007). Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS One, 2, e341.
37. Ohayon, M. M., Carskadon, M. A., Guilleminault, C., & Vitiello, M. V. (2004). Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: Developing normative sleep values across the human lifespan. Sleep, 27, 1255-1273.
38. Pace-Schott, E. F., & Spencer, R. M. C. (2013). Age-related changes in consolidation of perceptual and muscle-based learning of motor skills. Front Aging Neurosci, 5, 83.
39. Peters, K. R., Ray, L., Smith, V., & Smith, C. (2008). Changes in the density of stage 2 sleep spindles following motor learning in young and older adults. J Sleep Res, 17, 23-33.
40. Rasch, B., &Born, J. (2013). About Sleep's Role in Memory. Physiol Rev, 93, 681-766.
41. Robertson, E. M., Pascual-Leone, A., & Press, D. Z. (2004). Awareness modifies the skill-learning benefits of sleep. Curr Biol, 14, 208-212.
42. Rosekind, M., Smith, R., Miller, D., Co, E., Gregory, Webbon, L., Gander, P., &Lebacqz, J. (1995) Alertness management: Strategic naps in operational settings. J Sleep Res, 4, 62-66.
43. Schönauer, M., Grätsch, M., &Gais, S. (2014). Evidence for two distinct sleep-related long-term memory consolidation processes. Cortex, 63C, 68-78.
44. Scullin, M. K., & Bilwise, D. (2015). Sleep, cognition, and normal aging: Integrating a half-century of multidisciplinary research. Perspect Psychol Sci, 10, 97-137.
45. Siengsukon, C., &Boyd, L. A. (2008). Sleep enhances implicit motor skill learning in individuals poststroke. Top Stroke Rehabil, 15, 1-12.
46. Siengsukon, C., & Boyd, L. A. (2009). Sleep to learn after stroke: Implicit and explicit off-line motor learning. Neurosci Lett, 451, 1-5.
47. Siengsukon, C., & Boyd, L. A. (2009). Sleep enhances off-line spatial and temporal motor learning after stroke. Neurorehabil Neural Repair, 23, 327-335.
48. Siengsukon, C. F., & Al-Sharman, A. (2011). Sleep promotes offline enhancement of an explicitly learned discrete but not an explicitly learned continuous task. Nat Sci Sleep, 3, 39-46.
49. Spencer, R. M. C., Gouw, A. M., & Ivry, R. B. (2007). Age-related decline of sleep-dependent consolidation. Learn Mem, 14, 480-484.
50. Spencer, R. M. C., Sunm, M., & Ivry, R. B. (2006). Sleep-dependent consolidation of contextual learning. Curr Biol, 16, 1001-1005.
51. Takahashi, M., Nakata, A., Haratani, T., Ogawa, Y., & Arito, H. (2004). Post-lunch nap as a worksite intervention to promote alertness on the job. Ergonomics, 47, 1003-1013.
52. The Cochrane Collaboration. (2011) Cochrane Handbook for Systematic Reviews of Interventions, Version 5. edn. Wiley-Blackwell and Sally Green.
53. The GRADE working group (2014). URL www. gradeworkinggroup. org
54. Tucker, M., McKinley, S., & Stickgold, R. (2011). Sleep optimizes motor skill in older adults. J Am Geriatr Soc, 59, 603-609.
55. Van Cauter, E. (2000). Age-related changes in slow wave sleep and REM sleep and relationship with growth hormone and cortisol levels in healthy men. JAMA, 284, 861.
56. Vitiello, M. V. (2006). Sleep in normal aging. Sleep Med Clin, 1, 171-176.
57. Voelcker-Rehage, C. (2008). Motor-skill learning in older adults-a review of studies on age-related differences. Eur Rev Aging Phys Act, 5, 5-16.
58. Warby, S. C., Wendt, S. L., Welinder, P., Munk, E. G. S., Carrillo, O., Sorensen, H. B. D., Jennum, P., Peppard, P. E., Perona, P., & Mignot, E. (2014). Sleep-spindle detection: Crowdsourcing and evaluating performance of experts, non-experts and automated methods. Nat Methods, 11, 385-392.
59. Wilhelm, I., Diekelmann, S., Molzow, I., Ayoub, A., Mölle, M., & Born, J. (2011). Sleep selectively enhances memory expected to be of future relevance. J Neurosci, 31, 1563-1569.
60. Wilhelm, I., Metzkow-Mészáros, M., Knapp, S., & Born, J. (2012). Sleep-dependent consolidation of procedural motor memories in children and adults: The pre-sleep level of performance matters. Dev Sci, 15, 506-515.
61. Wilson, J. K., Baran, B., Pace-Schott, E. F., Ivry, R. B., & Spencer, R. M. C. (2012). Sleep modulates word-pair learning but not motor sequence learning in healthy older adults. Neurobiol Aging, 33, 991-1000.
62. Wolkove, N., Elkholy, O., Baltzan, M., & Palayew, M. (2007). Sleep and aging: 1. Sleep disorders commonly found in older people. CMAJ, 176, 1299-1304.
63. Zimerman, M., Nitsch, M., Giraux, P., Gerloff, C., Cohen, L. G., & Hummel, F. C. (2013). Neuroenhancement of the aging brain: Restoring skill acquisition in old subjects. Ann Neurol, 73, 10-15.