The Role of Sleep in Motor Sequence Consolidation: Stabilization Rather Than Enhancement

Sleep supports the consolidation of motor sequence memories, yet it remains unclear whether sleep stabilizes or actually enhances motor sequence performance. Here we assessed the time course of motor memory consolidation in humans, taking early boosts in performance into account and varying the time between training and sleep. Two groups of subjects, each participating in a short wake condition and a longer sleep condition, were trained on the sequential finger-tapping task in the evening and were tested (1) after wake intervals of either 30 min or 4 h and (2) after a night of sleep that ensued either 30 min or 4 h after training. The results show an early boost in performance 30 min after training and a subsequent decay across the 4 h wake interval. When sleep followed 30 min after training, post-sleep performance was stabilized at the early boost level. Sleep at 4 h after training restored performance to the early boost level, such that, 12 h after training, performance was comparable regardless of whether sleep occurred 30 min or 4 h after training. These findings indicate that sleep does not enhance but rather stabilizes motor sequence performance without producing additional gains.

[1]  P. Maquet,et al.  Early boost and slow consolidation in motor skill learning. , 2006, Learning & memory.

[2]  H. J. Eysenck,et al.  Reminiscence, Motivation, and Personality: A Case Study in Experimental Psychology , 1977 .

[3]  André Luxen,et al.  Recurrent boosting effects of short inactivity delays on performance: an ERPs study , 2009, BMC Research Notes.

[4]  M. Dresler,et al.  Sex and modulatory menstrual cycle effects on sleep related memory consolidation , 2012, Psychoneuroendocrinology.

[5]  Jeffrey D. Karpicke,et al.  Test-Enhanced Learning , 2006, Psychological science.

[6]  Christophe Phillips,et al.  Implicit Oculomotor Sequence Learning in Humans: Time Course of Offline Processing , 2022 .

[7]  R. Stickgold,et al.  Dissociable stages of human memory consolidation and reconsolidation , 2003, Nature.

[8]  Lisa Genzel,et al.  Impaired off-line memory consolidation in depression , 2010, European Neuropsychopharmacology.

[9]  R. Stickgold,et al.  Sleep and the time course of motor skill learning. , 2003, Learning & memory.

[10]  Sunbin Song,et al.  Practice and sleep form different aspects of skill , 2014, Nature Communications.

[11]  Tamar Flash,et al.  Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Alvaro Pascual-Leone,et al.  Current concepts in procedural consolidation , 2004, Nature Reviews Neuroscience.

[13]  R. Stickgold,et al.  Practice with Sleep Makes Perfect Sleep-Dependent Motor Skill Learning , 2002, Neuron.

[14]  I. Wilhelm,et al.  Sleep Selectively Enhances Memory Expected to Be of Future Relevance , 2011, The Journal of Neuroscience.

[15]  Timothy C Rickard,et al.  Sleep Does Not Enhance Motor Sequence Learning and Sumeet Gupta for Assistance with Data Collection; Daniel Bajic for Assistance with Programming; and John Wixted for Comments on an Earlier , 2008 .

[16]  Kimberly M. Fenn,et al.  Consolidating the Effects of Waking and Sleep on Motor-Sequence Learning , 2010, The Journal of Neuroscience.

[17]  Björn Rasch,et al.  Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory , 2009, Nature Neuroscience.

[18]  Jeffrey D. Karpicke,et al.  The Critical Importance of Retrieval for Learning , 2008, Science.

[19]  M. Desseilles,et al.  Both the Hippocampus and Striatum Are Involved in Consolidation of Motor Sequence Memory , 2008, Neuron.

[20]  Matthew P Walker,et al.  A refined model of sleep and the time course of memory formation. , 2005, The Behavioral and brain sciences.

[21]  E. Olivier,et al.  Role of the Primary Motor Cortex in the Early Boost in Performance Following Mental Imagery Training , 2011, PloS one.

[22]  E. Wolpert.  A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. , 1969 .

[23]  P. Maquet,et al.  Repetitive transcranial magnetic stimulation over the primary motor cortex disrupts early boost but not delayed gains in performance in motor sequence learning , 2008, The European journal of neuroscience.

[24]  Susanne Diekelmann,et al.  Sleep in children improves memory performance on declarative but not procedural tasks. , 2008, Learning & memory.

[25]  G. Tononi,et al.  Local sleep and learning , 2004, Nature.

[26]  J. Born,et al.  Sleep forms memory for finger skills , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[27]  H. Heuer,et al.  One night of total sleep deprivation impairs implicit learning in the serial reaction task, but not the behavioral expression of knowledge. , 2003, Neuropsychology.

[28]  J. Born,et al.  Motor Memory Consolidation in Sleep Shapes More Effective Neuronal Representations , 2005, The Journal of Neuroscience.

[29]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

[30]  A. Karni,et al.  Daytime sleep condenses the time course of motor memory consolidation , 2007, Nature Neuroscience.