Sleep‐dependent consolidation of procedural motor memories in children and adults: the pre‐sleep level of performance matters
Abstract
In striking contrast to adults, in children sleep following training a motor task did not induce the expected (offline) gain in motor skill performance in previous studies. Children normally perform at distinctly lower levels than adults. Moreover, evidence in adults suggests that sleep dependent offline gains in skill essentially depend on the pre‐sleep level of performance. Against this background, we asked whether improving children’s performance on a motor sequence learning task by extended training to levels approaching those of adults would enable sleep‐associated gains in motor skill in this age group also. Children (4–6 years) and adults (18–35 years) performed on the motor sequence learning task (button‐box task) before and after ∼2‐hour retention intervals including either sleep (midday nap) or wakefulness. Whereas one group of children and adults, respectively, received the standard amount of 10 blocks of training before retention intervals of sleep or wakefulness, a further group of children received an extended training on 30 blocks (distributed across 3 days). A further group of adults received a restricted training on only two blocks before the retention intervals. Children after standard training reached lowest performance levels, whereas in adults performance after standard training was highest. Children with extended training and adults after reduced training reached intermediate performance levels. Only at these intermediate performance levels did sleep induce significant gains in motor sequence skill, whereas performance did not benefit from sleep in the low‐performing children or in the high‐performing adults. Spindle counts in the post‐training nap were correlated with performance gains at retrieval only in the adults benefitting from sleep. We conclude that, across age groups, sleep induces the most robust gain in motor skill at an intermediate pre‐sleep performance level. In low‐performing children sleep‐dependent improvements in skill may be revealed only after enhancing the pre‐sleep performance level by extended training.
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Children aged 4-6 years who received high amounts of training in a finger-tapping task developed a significant gain in tapping skill across sleep, whereas low-performing children with standard training did not.
“Indeed, children (aged 4 -6 years) who received high amounts of training in a finger-tapping task did develop a significant gain in tapping skill across sleep, whereas no such gain was observed in low performing children who had received the standard amount of training (1320).”
From About Sleep's Role in Memory (2013) · cites this paper as [1320]
In the adults of that study, only the group with minimum training showed a consistent benefit from the nap.
“In the adults of this study, only the group with minimum training showed a consistent benefit from the nap.”
From About Sleep's Role in Memory (2013) · cites this paper as [1320]
Cites
The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research
Buysse, D. J., Reynolds, C. F., Monk, T. H., Berman, S. R., & Kupfer, D. J. (1989) · Psychiatry Research · doi:10.1016/0165-1781(89)90047-4 · Cited by 35,234 · see citing works
KAUFMAN, J., BIRMAHER, B., BRENT, D., RAO, U., FLYNN, C., MORECI, P., WILLIAMSON, D., & RYAN, N. (1997) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199707000-00021 · Cited by 10,148 · see citing works
Hobson, J. A. (1969) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(69)90021-2 · Cited by 5,215 · see citing works
Diekelmann, S., & Born, J. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2762 · Cited by 3,760 · see citing works
Self-citationOhayon, M. M., Carskadon, M. A., Guilleminault, C., & Vitiello, M. V. (2004) · Sleep · doi:10.1093/sleep/27.7.1255 · Cited by 3,349 · see citing works
Karni, A., Meyer, G., Rey-Hipolito, C., Jezzard, P., Adams, M. M., Turner, R., & Ungerleider, L. G. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.3.861 · Cited by 1,387 · see citing works
Interactive memory systems in the human brain
Poldrack, R. A., Clark, J., Paré-Blagoev, E. J., Shohamy, D., Creso Moyano, J., Myers, C., & Gluck, M. A. (2001) · Nature · doi:10.1038/35107080 · Cited by 1,132 · see citing works
Reorganization and plasticity in the adult brain during learning of motor skills
Doyon, J., & Benali, H. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.03.004 · Cited by 1,028 · see citing works
Dissociable stages of human memory consolidation and reconsolidation
Walker, M. P., Brakefield, T., Allan Hobson, J., & Stickgold, R. (2003) · Nature · doi:10.1038/nature01930 · Cited by 1,025 · see citing works
A neuropsychological theory of motor skill learning.
Willingham, D. B. (1998) · Psychological Review · doi:10.1037/0033-295x.105.3.558 · Cited by 798 · see citing works
Fogel, S. M., & Smith, C. T. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.003 · Cited by 628 · see citing works
Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep
Mölle, M., Marshall, L., Gais, S., & Born, J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10941.2002 · Cited by 617 · see citing works
Self-citationAn fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning
Schendan, H. E., Searl, M. M., Melrose, R. J., & Stern, C. E. (2003) · Neuron · doi:10.1016/s0896-6273(03)00123-5 · Cited by 610 · see citing works
Sleep forms memory for finger skills
Fischer, S., Hallschmid, M., Elsner, A. L., & Born, J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182178199 · Cited by 589 · see citing works
The whats and whens of sleep-dependent memory consolidation
Diekelmann, S., Wilhelm, I., & Born, J. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2008.08.002 · Cited by 566 · see citing works
Self-citationDaytime naps, motor memory consolidation and regionally specific sleep spindles
Nishida, M., & Walker, M. P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000341 · Cited by 531 · see citing works
Both the Hippocampus and Striatum Are Involved in Consolidation of Motor Sequence Memory
Albouy, G., Sterpenich, V., Balteau, E., Vandewalle, G., Desseilles, M., Dang-Vu, T., Darsaud, A., Ruby, P., Luppi, P.-H., Degueldre, C., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.02.008 · Cited by 463 · see citing works
Sleep and the Time Course of Motor Skill LearningPreprint
Walker, M. P., Brakefield, T., Seidman, J., Morgan, A., Hobson, J. A., & Stickgold, R. (2003) · Learning & Memory · doi:10.1101/lm.58503 · Cited by 457 · see citing works
Awareness Modifies the Skill-Learning Benefits of Sleep
Robertson, E. M., Pascual-Leone, A., & Press, D. Z. (2004) · Current Biology · doi:10.1016/j.cub.2004.01.027 · Cited by 450 · see citing works
Sleep selectively enhances memory expected to be of future relevance
Wilhelm, I., Diekelmann, S., Molzow, I., Ayoub, A., Mölle, M., & Born, J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3575-10.2011 · Cited by 397 · see citing works
Self-citationSleep-dependent learning and motor-skill complexity
Kuriyama, K., Stickgold, R., & Walker, M. P. (2004) · Learning & Memory · doi:10.1101/lm.76304 · Cited by 334 · see citing works
How sleep affects the developmental learning of bird song
Derégnaucourt, S., Mitra, P. P., Fehér, O., Pytte, C., & Tchernichovski, O. (2005) · Nature · doi:10.1038/nature03275 · Cited by 320 · see citing works
Brain plasticity related to the consolidation of motor sequence learning and motor adaptation
Debas, K., Carrier, J., Orban, P., Barakat, M., Lungu, O., Vandewalle, G., Tahar, A. H., Bellec, P., Karni, A., Ungerleider, L. G., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1013176107 · Cited by 295 · see citing works
Campbell, I. G., & Feinberg, I. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812947106 · Cited by 280 · see citing works
Sleep in children improves memory performance on declarative but not procedural tasks
Wilhelm, I., Diekelmann, S., & Born, J. (2008) · Learning & Memory · doi:10.1101/lm.803708 · Cited by 265 · see citing works
Self-citationThomas, K. M., Hunt, R. H., Vizueta, N., Sommer, T., Durston, S., Yang, Y., & Worden, M. S. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042304688 · Cited by 260 · see citing works
Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory
Rasch, B., Pommer, J., Diekelmann, S., & Born, J. (2009) · Nature Neuroscience · doi:10.1038/nn.2206 · Cited by 259 · see citing works
Self-citationDoyon, J., Korman, M., Morin, A., Dostie, V., Tahar, A. H., Benali, H., Karni, A., Ungerleider, L. G., & Carrier, J. (2009) · Experimental Brain Research · doi:10.1007/s00221-009-1748-y · Cited by 247 · see citing works
Implicit Sequence Learning in Children
Meulemans, T., der Linden, M. V., & Perruchet, P. (1998) · Journal of Experimental Child Psychology · doi:10.1006/jecp.1998.2442 · Cited by 231 · see citing works
Motor Sequence Learning Increases Sleep Spindles and Fast Frequencies in Post-Training Sleep
(2008) · Sleep · doi:10.5665/sleep/31.8.1149 · Cited by 213 · see citing works
Sleep Does Not Benefit Probabilistic Motor Sequence Learning
Song, S., Howard, J. H., & Howard, D. V. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2062-07.2007 · Cited by 195 · see citing works
Tamaki, M., Matsuoka, T., Nittono, H., & Hori, T. (2008) · SLEEP · doi:10.1093/sleep/31.2.204 · Cited by 171 · see citing works
Sleep does not enhance motor sequence learning.
Rickard, T. C., Cai, D. J., Rieth, C. A., Jones, J., & Ard, M. C. (2008) · Journal of Experimental Psychology: Learning, Memory, and Cognition · doi:10.1037/0278-7393.34.4.834 · Cited by 171 · see citing works
The sleeping child outplays the adult's capacity to convert implicit into explicit knowledge
Wilhelm, I., Rose, M., Imhof, K. I., Rasch, B., Büchel, C., & Born, J. (2013) · Nature Neuroscience · doi:10.1038/nn.3343 · Cited by 170 · see citing works
Self-citationFletcher, P. C., Zafiris, O., Frith, C., Honey, R. A. E., Corlett, P. R., Zilles, K., & Fink, G. R. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh201 · Cited by 156 · see citing works
Hauptmann, B., Reinhart, E., Brandt, S. A., & Karni, A. (2005) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2005.01.012 · Cited by 151 · see citing works
Fischer, S., Wilhelm, I., & Born, J. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.2.214 · Cited by 142 · see citing works
Self-citationSleep-Dependent Consolidation of Contextual Learning
Spencer, R. M. C., Sunm, M., & Ivry, R. B. (2006) · Current Biology · doi:10.1016/j.cub.2006.03.094 · Cited by 138 · see citing works
Shanks, D. R., & Johnstone, T. (1999) · Journal of Experimental Psychology: Learning, Memory, and Cognition · doi:10.1037/0278-7393.25.6.1435 · Cited by 135 · see citing works
Shanks, D. R., & Johnstone, T. (1999) · Journal of Experimental Psychology Learning Memory and Cognition · doi:10.1037//0278-7393.25.6.1435 · Cited by 134 · see citing works
Rauchs, G., Feyers, D., Landeau, B., Bastin, C., Luxen, A., Maquet, P., & Collette, F. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3972-10.2011 · Cited by 121 · see citing works
Sleep in children enhances preferentially emotional declarative but not procedural memories
Prehn-Kristensen, A., Göder, R., Chirobeja, S., Breßmann, I., Ferstl, R., & Baving, L. (2009) · Journal of Experimental Child Psychology · doi:10.1016/j.jecp.2009.01.005 · Cited by 117 · see citing works
Reduced Susceptibility to Interference in the Consolidation of Motor Memory before Adolescence
Dorfberger, S., Adi-Japha, E., & Karni, A. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000240 · Cited by 109 · see citing works
How do I remember? Let me count the ways
Stickgold, R. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2009.05.004 · Cited by 90 · see citing works
Sun, R., Zhang, X., Slusarz, P., & Mathews, R. C. (2006) · Neural Networks · doi:10.1016/j.neunet.2006.07.002 · Cited by 74 · see citing works
Time of day accounts for overnight improvement in sequence learningPreprint
Keisler, A., Ashe, J., & Willingham, D. T. (2007) · Learning & Memory · doi:10.1101/lm.751807 · Cited by 56 · see citing works
Reconsidering the role of sleep for motor memory.
Cai, D. J., & Rickard, T. C. (2009) · Behavioral Neuroscience · doi:10.1037/a0017672 · Cited by 46 · see citing works
Grouping of MEG gamma oscillations by EEG sleep spindles
Ayoub, A., Mölle, M., Preissl, H., & Born, J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.08.023 · Cited by 39 · see citing works
Self-citation
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Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Self-citationThe Consolidation and Transformation of Memory
Dudai, Y., Karni, A., & Born, J. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.004 · Cited by 741 · see citing works
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Kurdziel, L., Duclos, K., & Spencer, R. M. C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1306418110 · Cited by 266 · see citing works
Generalization of word meanings during infant sleep
Friedrich, M., Wilhelm, I., Born, J., & Friederici, A. D. (2015) · Nature Communications · doi:10.1038/ncomms7004 · Cited by 176 · see citing works
Self-citationSleep and memory in mammals, birds and invertebrates
Vorster, A. P., & Born, J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.020 · Cited by 169 · see citing works
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Wilhelm, I., Prehn-Kristensen, A., & Born, J. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.002 · Cited by 161 · see citing works
Self-citationWamsley, E. J., & Stickgold, R. (2019) · Journal of Sleep Research · doi:10.1111/jsr.12749 · Cited by 90 · see citing works
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Urbain, C., De Tiège, X., Op De Beeck, M., Bourguignon, M., Wens, V., Verheulpen, D., Van Bogaert, P., & Peigneux, P. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.03.055 · Cited by 44 · see citing works
Slow wave sleep in naps supports episodic memories in early childhood
Lokhandwala, S., & Spencer, R. M. C. (2021) · Developmental Science · doi:10.1111/desc.13035 · Cited by 41 · see citing works
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Wang, J.-Y., Weber, F. D., Zinke, K., Inostroza, M., & Born, J. (2018) · Child Development · doi:10.1111/cdev.12839 · Cited by 29 · see citing works
Self-citation
- Authors
- Wilhelm, I., Metzkow‐Mészàros, M., Knapp, S., & Born, J.
- Affiliations
- University of Tübingen (DE)
- Martin Luther University Halle-Wittenberg (DE)
- Corresponding author
- Wilhelm, Ines
- ORCID
- Wilhelm, Ines
- Venue
- Developmental Science
- Publisher
- Wiley
- Published
- 2012-04-05
- Volume
- 15
- Issue
- 4
- Pages
- 506-515
- ISSN
- 1363-755X (ISSN-L)
- 1467-7687
- OpenAlex
- W1806129265
- Cited by
- 143
- References
- 48
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 10 · 2023: 6 · 2022: 5 · 2021: 11 · 2020: 14 · 2019: 10 · 2018: 9 · 2017: 17 · 2016: 17 · 2015: 12 · 2014: 12 · 2013: 12 · 2012: 1
- FWCI
- 6.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Developmental Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Keywords
- sleep-dependent memory consolidation, procedural memory, motor skill learning, children, age differences, motor sequence learning, extended training, retention interval
- MeSH terms
- Adult, Child, Child, Preschool, Female, Humans, Learning, Male, Memory, Motor Skills, Retention, Psychology, Sleep, Task Performance and Analysis, Time Factors, Wakefulness, Polysomnography, Young Adult
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