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Research Article

Learning by observation requires an early sleep window

Ysbrand D. Van Der Werf, Els Van Der Helm, Menno M. Schoonheim, Arne Ridderikhoff, and Eus J. W. Van Someren
  1. aDepartment of Sleep and Cognition, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA, Amsterdam, The Netherlands;
  2. bDepartments of Clinical Neurophysiology, Neurology and Medical Psychology and Anatomy and Neurosciences, VU University Medical Center, P.O. Box 7057, 1007 MB, Amsterdam, The Netherlands; and
  3. cFaculty of Human Movement Sciences, VU University, Van der Boechorststraat 9, 1081 BT, Amsterdam, The Netherlands

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PNAS November 10, 2009 106 (45) 18926-18930; https://doi.org/10.1073/pnas.0901320106
Ysbrand D. Van Der Werf
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  • For correspondence: y.van.der.werf@nin.knaw.nl
Els Van Der Helm
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Menno M. Schoonheim
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Arne Ridderikhoff
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Eus J. W. Van Someren
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  1. Edited by Brenda Milner, McGill University, Montreal, Canada, and approved July 24, 2009 (received for review February 9, 2009)

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Abstract

Numerous studies have shown that sleep enhances memory for motor skills learned through practice. Motor skills can, however, also be learned through observation, a process possibly involving the mirror neuron system. We investigated whether motor skill enhancement through prior observation requires sleep to follow the observation, either immediately or after a delay, to consolidate the procedural memory. Sequence-specific fingertapping performance was tested in 64 healthy subjects in a balanced design. Electromyography verified absence of overt or subliminal hand muscle activations during observation. The results show that immediate sleep is necessary for the enhancement of a motor skill through prior observation. Immediate sleep improved the speed of subsequent performance by 22 ± 11% (mean ± SEM) (P = 0.04) and reduced the error rate by 42 ± 19% (P = 0.02). In contrast, no performance gains occurred if sleep was initiated more than 12 h after observation. A second study on 64 subjects ruled out explicit familiarity with the sequence or the spatiotemporal rhythm of the sequence to underlie performance improvements. The sleep-dependent observational motor learning enhancement is at least similar to that previously reported for implicit and declarative memory. The apparent prerequisite of observing real movements indicates that subjects transfer experience obtained through observation of movements to subsequent self-initiated movements, in the absence of practice. Moreover, the consolidation of this transfer requires an early sleep window. These findings could improve learning new motor skills in athletes and children, but also in patients having to remaster skills following stroke or injury.

  • circadian rhythms
  • memory consolidation
  • mirror neurons
  • offline improvement

Footnotes

  • 1To whom correspondence should be addressed. E-mail: y.van.der.werf{at}nin.knaw.nl
  • Author contributions: Y.D.V.D.W., A.R., and E.J.W.V.S. designed research; Y.D.V.D.W., E.V.D.H., M.M.S., and A.R. performed research; Y.D.V.D.W., E.V.D.H., A.R., and E.J.W.V.S. analyzed data; and Y.D.V.D.W., E.V.D.H., and E.J.W.V.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

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Learning by observation requires an early sleep window
Ysbrand D. Van Der Werf, Els Van Der Helm, Menno M. Schoonheim, Arne Ridderikhoff, Eus J. W. Van Someren
Proceedings of the National Academy of Sciences Nov 2009, 106 (45) 18926-18930; DOI: 10.1073/pnas.0901320106

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Learning by observation requires an early sleep window
Ysbrand D. Van Der Werf, Els Van Der Helm, Menno M. Schoonheim, Arne Ridderikhoff, Eus J. W. Van Someren
Proceedings of the National Academy of Sciences Nov 2009, 106 (45) 18926-18930; DOI: 10.1073/pnas.0901320106
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Proceedings of the National Academy of Sciences: 106 (45)
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