Abstract
Sleep is beneficial for performance across a range of memory tasks in young adults, but whether memories are similarly consolidated in older adults is less clear. Performance benefits have been observed following sleep in older adults for declarative learning tasks, but this benefit may be reduced for non-declarative, motor skill learning tasks. To date, studies of sleep-dependent consolidation of motor learning in older adults are limited to motor sequence tasks. To examine whether reduced sleep-dependent consolidation in older adults is generalizable to other forms of motor skill learning, we examined performance changes over intervals of sleep and wake in young (n = 62) and older adults (n = 61) using a mirror-tracing task, which assesses visuo-motor adaptation learning. Participants learned the task either in the morning or in evening, and performance was assessed following a 12-h interval containing overnight sleep or daytime wake. Contrary to our prediction, both young adults and older adults exhibited sleep-dependent gains in visuo-motor adaptation. There was a correlation between performance improvement over sleep and percent of the night in non-REM stage 2 sleep. These results indicate that motor skill consolidation remains intact with increasing age although this relationship may be limited to specific forms of motor skill learning.
Similar content being viewed by others
References
Barakat M, Carrier J, Debas K, Lungu O, Fogel S, Vandewalle G, Doyon J (2013) Sleep spindles predict neural and behavioral changes in motor sequence consolidation. Hum Brain Mapp 34:2918–2928
Brown RM, Robertson EM, Press DZ (2009) Sequence skill acquisition and off-line learning in normal aging. PLoS ONE 4:e6683
Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 2:193–213
Doyon J, Penhune V, Ungerleider LG (2003) Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41:252–262
Fischer S, Hallschmid M, Elsner AL, Born J (2002). Sleep forms memory for finger skills. Proc Nat Acad Sci USA 99:11987-11991
Fogel SM, Nader R, Cote KA, Smith CT (2007) Sleep spindles and learning potential. Behav Neurosci 121:1–10
Fogel SM, Martin N, Lafortune M, Barakat M, Debas K, Laventure S, Carrier J (2012) NREM sleep oscillations and brain plasticity in aging. Front Neurol 3:176
Fogel SM, Albouy G, Vien C, Popovicci R, King BR, Hoge R, Doyon J (2014) fMRI and sleep correlates of the age-related impairment in motor memory consolidation. Hum Brain Mapp 35:3625–3645
Gerrard JL, Burke SN, McNaughton BL, Barnes CA (2008) Sequence reactivation in the hippocampus is impaired in aged rats. J Neurosci 28:7883–7890
Gudberg C, Wulff K, Johansen-Berg H (2014) Sleep-dependent motor memory consolidation in older adults depends on task demands. Neurobiol Aging 36:1409–1416
Hoddes E, Zarcone V, Smythe H, Phillips R, Dement WC (1973) Quantification of sleepiness: a new approach. Psychophysiology 10:431–436
Horne JA, Ostberg O (1976) A self-assessment questionnaire to determine morningness–eveningness in human circadian rhythms. Int J Chronobiol 4:97–110
Howard DV, Howard JH (1989) Age differences in learning serial patterns: direct versus indirect measures. Psychol Aging 4:357–364
Javadi AH, Walsh V, Lewis PA (2011) Offline consolidation of procedural skill learning is enhanced by negative emotional content. Exp Brain Res 208:507–517
Johns MW (1994) Sleepiness in different situations measured by the Epworth Sleepiness Scale. Sleep 17:703–710
King BR, Fogel SM, 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
Laforce R, Doyon J (2002) Differential role for the striatum and cerebellum in response to novel movements using a motor learning paradigm. Neuropsychologia 40:512–517
Maquet P, Schwartz S, Passingham R, Frith C (2003a) Sleep-related consolidation of a visuomotor skill: brain mechanisms as assessed by functional magnetic resonance imaging. J Neurosci 23:1432–1440
Maquet P, Schwartz S, Passingham R, Frith C (2003b) Sleep-related consolidation of a visuomotor skill: brain mechanisms as assessed by functional magnetic resonance imaging. J Neurosci 23:1432–1440
Miall RC, Imamizu H, Miyauchi S (2000) Activation of the cerebellum in coordinated eye and hand tracking movements: an fMRI study. Exp Brain Res 135:22–33
Morin A, Doyon J, Dostie V, Barakat M, Tahar AH, Korman M, et al. (2008). Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep. Sleep 31:1149–1156
Pace-Schott E, Spencer RMC (2014a) Sleep and cognition in aging and dementia. In: Abel T, Benca R, Meerlo P (eds) Sleep, neuronal plasticity and brain function. Springer, New York
Pace-Schott E, Spencer RMC (2014b) Sleep loss in older adults: effects on waking performance and sleep-dependent consolidation with healthy aging and insomnia. In: Bianchi MT (ed) Sleep deprivation and disease: effects on the body, brain and behavior. Springer, New York
Peters KR, 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
Plihal W, Born J (1997) Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci 9:534–547
Reis J, Schambra HM, Cohen LG, Buch ER, Fritsch B, Zarahn E et al (2009) Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc Natl Acad Sci USA 106:1590–1595
Schredl M, Erlacher D (2007) REM sleep and visuo-motor skill learning: a correlational study. Sleep Hypn 9:52
Siengsukon CF, Boyd LA (2008) Sleep enhances implicit motor skill learning in individuals poststroke. Top Stroke Rehabil 15:1–12
Siengsukon CF, Boyd LA (2009) Sleep to learn after stroke: implicit and explicit off-line motor learning. Neurosci Lett 451:1–5
Silber MH, Ancoli-Israel S, Bonnet MH (2007) The visual scoring of sleep in adults. J Clin Sleep Med 3:121–131
Smith C (1995) Sleep states and memory processes. Behav Brain Res 69:137–145
Smith C, MacNeill C (1994) Impaired motor memory for a pursuit rotor task following Stage 2 sleep loss in college students. J sleep res 3:206-213
Spencer RMC, Gouw AM, Ivry RB (2007) Age-related decline of sleep-dependent consolidation. Learn Mem 14:480–484
Stickgold R (2005) Sleep-dependent memory consolidation. Nature 437:1272–1278
Tamaki M, Matsuoka T, Nittono H, Hori T (2008) Fast sleep spindle (13–15 Hz) activity correlates with sleep-dependent improvement in visuomotor performance. Sleep 31:204–211
Terpening Z, Naismith S, Melehan K, Gittins C, Bolitho S, Lewis SJ (2013) The contribution of nocturnal sleep to the consolidation of motor skill learning in healthy ageing and Parkinson’s disease. J Sleep Res 22:398–405
Tucker M, McKinley S, Stickgold R (2011) Sleep optimizes motor skill in older adults. J Am Geriatr Soc 59:603–609
Walker MP, Brakefield T, Morgan A, Hobson JA, Stickgold R (2002) Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35:205–211
Wilson JK, Baran B, Pace-Schott EF, Ivry RB, Spencer RMC (2012) Sleep modulates word-pair learning but not motor sequence learning in healthy older adults. Neurobiol Aging 33:991–1000
Acknowledgments
The authors acknowledge the work of Torey Davis in preparing Fig. 1. This work was supported by National Institutes of Health R01AG040133 awarded to RMC Spencer.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mantua, J., Baran, B. & Spencer, R.M.C. Sleep benefits consolidation of visuo-motor adaptation learning in older adults. Exp Brain Res 234, 587–595 (2016). https://doi.org/10.1007/s00221-015-4490-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-015-4490-7