Developmental Differences in Sleep's Role for Implicit Off-line Learning: Comparing Children with Adults
Abstract
Sleep crucially contributes to the off-line consolidation of memories. Although this view was confirmed in numerous studies in adults, it is not known whether it can be generalized to sleep during development. Here, we examined effects of sleep on implicit memory formation considered of particular relevance in children, because brain structures underlying implicit learning develop earlier in ontogeny than structures supporting explicit learning. Subjects were 7- to 11-year-old children (n = 14) and 20- to 30-year-old adults (n = 12) tested on a serial reaction time task before (learning) and after (retest) equal length retention periods of overnight sleep and daytime wakefulness. At learning, after eight training blocks, all subjects had acquired implicit knowledge of the probabilistic rules underlying the sequential stimulus materials, as indicated by a substantial difference in response time to grammatical versus nongrammatical trials in two test blocks that followed the training blocks. At learning, this response time difference was greater in children (48.49 ± 6.08 msec) than adults (28.02 ± 3.65 msec, p < .01), but did not differ between sleep and wake retention conditions in either age group. Consistent with previous studies, retesting in the adults revealed that the reaction time differences between grammatical and nongrammatical trials increased by 9.78 ± 4.82 msec after sleep, but decreased by −12.76 ± 5.49 msec after the wake retention period (p < .01). Contrary to this finding in adults, sleep in children did not lead to an increase, but to a decrease in the reaction time difference averaging −26.68 ± 12.25 msec (p < .05), whereas across the wake retention interval the reaction time difference remained nearly unchanged. The sleep-dependent deterioration in measures of implicit sequence knowledge in children was in striking contrast to the gain of such knowledge in the adults during sleep (p < .01). Our findings indicate that the functional role of sleep in implicit memory consolidation depends on age. We speculate that the overnight decrease of implicit knowledge in children reflects a preferential effect of sleep toward the enhancement of explicit aspects of task performance that interferes with implicit performance gains.
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Sleep-dependent gains in skills are more robust under explicit learning conditions than under implicit learning conditions.
“First, sleep-dependent gains in skills are more robust under explicit learning conditions (i.e., the subjects are aware about the skill to be acquired) (383, 664, 1285) compared with implicit learning conditions (385,1003,1122,1128).”
From About Sleep's Role in Memory (2013) · cites this paper as [385]
The majority of studies on sleep-dependent procedural memory formation in children indicated an impairing rather than improving effect of sleep on skill, similar to findings in juvenile songbirds where overnight sleep deteriorated tutored song performance.
“In fact, the majority of studies on sleepdependent procedural memory formation in children indicated an impairing rather than improving effect of sleep on skill (385, 947, 949, 1318), remarkably similar to findings in juvenile song birds where overnight sleep likewise deteriorated performance on the tutored song (280).”
From About Sleep's Role in Memory (2013) · cites this paper as [385]
In children, skill performance is generally much slower, less accurate, and less automated than in adults, particularly in the initial stage of training.
“In children, skill performance is generally much slower, less accurate, and less automated than in adults, particularly in the initial stage of training (318, 385, 1185), which gives rise to the question of whether sleep enhances skill memories also in children if presleep performance is improved to a level comparable with that in adults.”
From About Sleep's Role in Memory (2013) · cites this paper as [385]
The lack of sleep-dependent gains in skill performance in children might be ascribed to a competitive interaction between declarative and procedural memory systems.
“Alternatively, the lack of sleep-dependent gains in skill performance in children might be ascribed to a competitive interaction between declarative and procedural memory systems (385, 1318).”
From About Sleep's Role in Memory (2013) · cites this paper as [385]
Studies examining procedural memories consistently demonstrated that in children, unlike in adults, posttraining sleep does not produce a robust improvement of skill.
“In contrast to the strong beneficial effects of non-REM sleep on the consolidation of declarative memory in children, studies examining procedural memories consistently demonstrated that in children, unlike in adults, posttraining sleep does not produce a robust improvement of skill.”
From About Sleep's Role in Memory (2013) · cites this paper as [385]
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Self-citationWilhelm, I., Metzkow‐Mészàros, M., Knapp, S., & Born, J. (2012) · Developmental Science · doi:10.1111/j.1467-7687.2012.01146.x · Cited by 143 · see citing works
Self-citationDurrant, S. J., Cairney, S. A., & Lewis, P. A. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs244 · Cited by 124 · 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
Prehn-Kristensen, A., Molzow, I., Munz, M., Wilhelm, I., Müller, K., Freytag, D., Wiesner, C. D., & Baving, L. (2011) · Research in Developmental Disabilities · doi:10.1016/j.ridd.2011.06.021 · Cited by 62 · see citing works
Self-citationPeiffer, A., Brichet, M., De Tiège, X., Peigneux, P., & Urbain, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-66880-3 · Cited by 34 · see citing works
Sleep strengthens predictive sequence coding
Lutz, N. D., Wolf, I., Hübner, S., Born, J., & Rauss, K. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1352-18.2018 · Cited by 27 · see citing works
Self-citationMikoteit, T., Brand, S., Beck, J., Perren, S., von Wyl, A., von Klitzing, K., Holsboer-Trachsler, E., & Hatzinger, M. (2012) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2011.562241 · Cited by 21 · see citing works
Occipital sleep spindles predict sequence learning in a visuo-motor task
Lutz, N. D., Admard, M., Genzoni, E., Born, J., & Rauss, K. (2021) · SLEEP · doi:10.1093/sleep/zsab056 · Cited by 12 · see citing works
- Authors
- Fischer, S., Wilhelm, I., & Born, J.
- Affiliations
- Innsbruck Medical University (AT)
- University of Lübeck (DE)
- 2University of Lübeck, Lübeck, Germany
- ORCID
- Wilhelm, Ines
- Venue
- Journal of Cognitive Neuroscience
- Publisher
- MIT Press
- Published
- 2007-02-01
- Volume
- 19
- Issue
- 2
- Pages
- 214-227
- ISSN
- 0898-929X (ISSN-L)
- 1530-8898
- OpenAlex
- W1982430441
- Cited by
- 142
- References
- 84
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 5 · 2023: 4 · 2022: 8 · 2021: 7 · 2020: 5 · 2019: 9 · 2018: 7 · 2017: 5 · 2016: 9 · 2015: 12 · 2014: 15 · 2013: 11 · 2012: 12
- FWCI
- 2.66
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Cognitive Neuroscience (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 › Memory Processes and Influences
- Keywords
- sleep-dependent memory consolidation, implicit learning, offline learning, children versus adults, ontogeny, serial reaction time task, explicit learning, nocturnal sleep, age differences
- MeSH terms
- Adult, Aging, Analysis of Variance, Child, Female, Humans, Male, Memory, Neuropsychological Tests, Reaction Time, Serial Learning, Sleep, Task Performance and Analysis
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