Sleep Does Not Benefit Probabilistic Motor Sequence Learning

It has become widely accepted that sleep-dependent consolidation occurs for motor sequence learning based on studies using finger-tapping tasks. Studies using another motor sequence learning task [the serial response time task (SRTT)] have portrayed a more nuanced picture of off-line consolidation, involving both sleep-dependent and daytime consolidation, as well as modifying influences of explicit awareness. The present study used a variant of the SRTT featuring probabilistic sequences to investigate off-line consolidation. Probabilistic sequences confer two advantages: first, spontaneous explicit awareness does not occur, and second, sequence learning measures are continuous, making it easier to separate general skill from sequence-specific learning. We found that sleep did not enhance general skill or sequence-specific learning. In contrast, daytime enhancement occurred for general skill but not for sequence-specific learning. Overall, these results suggest that motor learning does not always undergo consolidation with sleep.

[1]  Jan Born,et al.  Implicit Learning–Explicit Knowing: A Role for Sleep in Memory System Interaction , 2006, Journal of Cognitive Neuroscience.

[2]  M. Gluck,et al.  Interactive memory systems in the human brain , 2001, Nature.

[3]  R. Stickgold Sleep-dependent memory consolidation , 2005, Nature.

[4]  Stefan Fischer,et al.  Developmental Differences in Sleep's Role for Implicit Off-line Learning: Comparing Children with Adults , 2007, Journal of Cognitive Neuroscience.

[5]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

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

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

[8]  C. Stern,et al.  An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning , 2003, Neuron.

[9]  J. Born,et al.  Odor Cues During Slow-Wave Sleep Prompt Declarative Memory Consolidation , 2007, Science.

[10]  B. Nolan Boosting slow oscillations during sleep potentiates memory , 2008 .

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

[12]  Alvaro Pascual-Leone,et al.  Off-line learning of motor skill memory: a double dissociation of goal and movement. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  E. Wamsley,et al.  A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory , 2006, Neurobiology of Learning and Memory.

[14]  Daniel B. Willingham,et al.  Patterns of interference in sequence learning and prism adaptation inconsistent with the consolidation hypothesis. , 2002, Learning & memory.

[15]  Sunbin Song,et al.  Implicit probabilistic sequence learning is independent of explicit awareness. , 2007, Learning & memory.

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

[17]  Robert Stickgold,et al.  Cerebral Cortex doi:10.1093/cercor/bhi043 The Functional Anatomy of Sleep-dependent Visual Skill Learning , 2005 .

[18]  C. Degueldre,et al.  Are Spatial Memories Strengthened in the Human Hippocampus during Slow Wave Sleep? , 2004, Neuron.

[19]  J. Hobson,et al.  Visual Discrimination Task Improvement: A Multi-Step Process Occurring During Sleep , 2000, Journal of Cognitive Neuroscience.

[20]  R. Stickgold,et al.  Posttraining Sleep Enhances Automaticity in Perceptual Discrimination , 2004, Journal of Cognitive Neuroscience.

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

[22]  Daniel B. Willingham,et al.  The Relation Between Implicit and Explicit Learning: Evidence for Parallel Development , 1999 .

[23]  J. H. Howard,et al.  Age differences in implicit learning of higher order dependencies in serial patterns. , 1997, Psychology and aging.

[24]  C. Pavlides,et al.  Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  Tim Curran,et al.  Higher-Order Associative Learning in Amnesia: Evidence from the Serial Reaction Time Task , 1997, Journal of Cognitive Neuroscience.

[26]  M. Nissen,et al.  Attentional requirements of learning: Evidence from performance measures , 1987, Cognitive Psychology.

[27]  Richard B. Ivry,et al.  Sleep-Dependent Consolidation of Contextual Learning , 2006, Current Biology.

[28]  J. Hobson,et al.  Visual discrimination learning requires sleep after training , 2000, Nature Neuroscience.

[29]  D. Howard,et al.  Implicit sequence learning: effects of level of structure, adult age, and extended practice. , 2004, Psychology and aging.

[30]  Á. Pascual-Leone,et al.  Awareness Modifies the Skill-Learning Benefits of Sleep , 2004, Current Biology.

[31]  Luis Jiménez,et al.  Which Attention Is Needed for Implicit Sequence Learning , 1999 .

[32]  R. Stickgold,et al.  Replaying the game: hypnagogic images in normals and amnesics. , 2000, Science.

[33]  J. Born,et al.  Early sleep triggers memory for early visual discrimination skills , 2000, Nature Neuroscience.

[34]  A. Karni,et al.  Dependence on REM sleep of overnight improvement of a perceptual skill. , 1994, Science.

[35]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[36]  Matthew S. Cain,et al.  A failure of sleep-dependent procedural learning in chronic, medicated schizophrenia , 2004, Biological Psychiatry.

[37]  K. Junghanns,et al.  Daytime naps improve procedural motor memory. , 2006, Sleep medicine.

[38]  J. Horne,et al.  A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. , 1976, International journal of chronobiology.

[39]  Á. Pascual-Leone,et al.  Off-Line Learning and the Primary Motor Cortex , 2005, The Journal of Neuroscience.

[40]  Edwin M. Robertson,et al.  Motor sequence consolidation: constrained by critical time windows or competing components , 2007, Experimental Brain Research.

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

[42]  Roger W. Schvaneveldt,et al.  Attention and probabilistic sequence learning , 1998 .

[43]  Luis Jiménez,et al.  Qualitative differences between implicit and explicit sequence learning. , 2006, Journal of experimental psychology. Learning, memory, and cognition.

[44]  K. Nakayama,et al.  Sleep-dependent learning: a nap is as good as a night , 2003, Nature Neuroscience.

[45]  J. Born,et al.  Sleep inspires insight , 2004, Nature.

[46]  Daniel J Buysse,et al.  The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research , 1989, Psychiatry Research.

[47]  Edwin M Robertson,et al.  Understanding Consolidation through the Architecture of Memories , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[48]  R. Passingham,et al.  Sleep-Related Consolidation of a Visuomotor Skill: Brain Mechanisms as Assessed by Functional Magnetic Resonance Imaging , 2003, The Journal of Neuroscience.

[49]  Alvaro Pascual-Leone,et al.  The time course of off-line motor sequence learning. , 2005, Brain research. Cognitive brain research.

[50]  A. A. Levin,et al.  The restorative effect of naps on perceptual deterioration , 2002, Nature Neuroscience.

[51]  R. Stickgold,et al.  Sleep-dependent learning and motor-skill complexity. , 2004, Learning & memory.