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Consolidating the Effects of Waking and Sleep on Motor-Sequence Learning
Open accessAbstract
Sleep is widely believed to play a critical role in memory consolidation. Sleep-dependent consolidation has been studied extensively in humans using an explicit motor-sequence learning paradigm. In this task, performance has been reported to remain stable across wakefulness and improve significantly after sleep, making motor-sequence learning the definitive example of sleep-dependent enhancement. Recent work, however, has shown that enhancement disappears when the task is modified to reduce task-related inhibition that develops over a training session, thus questioning whether sleep actively consolidates motor learning. Here we use the same motor-sequence task to demonstrate sleep-dependent consolidation for motor-sequence learning and explain the discrepancies in results across studies. We show that when training begins in the morning, motor-sequence performance deteriorates across wakefulness and recovers after sleep, whereas performance remains stable across both sleep and subsequent waking with evening training. This pattern of results challenges an influential model of memory consolidation defined by a time-dependent stabilization phase and a sleep-dependent enhancement phase. Moreover, the present results support a new account of the behavioral effects of waking and sleep on explicit motor-sequence learning that is consistent across a wide range of tasks. These observations indicate that current theories of memory consolidation that have been formulated to explain sleep-dependent performance enhancements are insufficient to explain the range of behavioral changes associated with sleep.
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“In fact, at a purely behavioral level, numerous studies have demonstrated that sleep after learning benefits declarative (17,18,60,63,79,290,326,327,343,348,350,376,408,427,431,478,479,547,560,571,574,592,603,682,732,735,861,898,930,932,959,1069,1172,1192,1217,1274,1276,1278,1282,1302) as well as nondeclarative kinds of procedural memory (135,147,164,311,322,374,383,435,447,563,602,631,664,679,733”
From About Sleep's Role in Memory (2013) · cites this paper as [135]
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Cites
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Self-citationSleep and the Time Course of Motor Skill LearningPreprint
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Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783
“In fact, at a purely behavioral level, numerous studies have demonstrated that sleep after learning benefits declarative (17, 18, 60, 63, 79, 290, 326, 327, 343, 348, 350, 376, 408, 427, 431, 478, 479, 547, 560, 571, 574, 592, 603, 682, 732, 735, 861, 898, 930, 932, 959, 1069, 1172, 1192, 1217, 1274, 1276, 1278, 1282,…”
Neuroplasticity Subserving Motor Skill Learning
Dayan, E., & Cohen, L. G. (2011) · Neuron · doi:10.1016/j.neuron.2011.10.008 · Cited by 1,408
Consolidation alters motor sequence-specific distributed representations
Pinsard, B., Boutin, A., Gabitov, E., Lungu, O., Benali, H., & Doyon, J. (2019) · eLife · doi:10.7554/elife.39324 · Cited by 1,066
Sleep-dependent memory triage: evolving generalization through selective processing
Stickgold, R., & Walker, M. P. (2013) · Nature Neuroscience · doi:10.1038/nn.3303 · Cited by 755
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644
Metadata
- Authors
- Brawn, T. P., Fenn, K. M., Nusbaum, H. C., & Margoliash, D.
- Affiliations
- University of Chicago (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-10-20
- Volume
- 30
- Issue
- 42
- Pages
- 13977-13982
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2978076
- OpenAlex
- W2105690873
- Cited by
- 181
- References
- 20
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 11 · 2023: 12 · 2022: 8 · 2021: 7 · 2020: 27 · 2019: 12 · 2018: 9 · 2017: 17 · 2016: 9 · 2015: 12 · 2014: 13 · 2013: 17 · 2012: 11
- FWCI
- 6.21
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (R01MH059831, MH059831)
- National Institute on Deafness and Other Communication Disorders (R01DC007206, DC 007206)
- 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, motor sequence learning, explicit motor learning, training time of day
- MeSH terms
- Adolescent, Adult, Circadian Rhythm, Female, Humans, Male, Memory, Motor Skills, Psychomotor Performance, Reaction Time, Serial Learning, Sleep, Wakefulness, Young Adult
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