Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance

When do learning-related changes in performance occur? Here we show that the knowledge of a sequence of movements evolves through several distinctive phases that depend on two critical factors: the amount of practice as well as the passage of time. Our results show the following. (i) Within a given session, large performance gains constituted a signature for motor novelty. Such gains occurred only for newly introduced conditions irrespective of the absolute level of performance. (ii) A single training session resulted in both immediate but also time-dependent, latent learning hours after the termination of practice. Time in sleep determined the time of expression of these delayed gains. Moreover, the delayed gains were sequence-specific, indicating a qualitative change in the representation of the task within 24 h posttraining. (iii) Prolonged training resulted in additional between-session gains that, unlike the effects of a single training session, were confined to the trained hand. Thus, the effects of multisession training were qualitatively different than the immediate and time-dependent effects of a single session. Altogether, our results indicate multiple time-dependent shifts in the representation of motor experience during the acquisition of skilled performance.

[1]  D. Zipser,et al.  A spiking network model of short-term active memory , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[3]  J. Tracy,et al.  A comparison of 'Early' and 'Late' stage brain activation during brief practice of a simple motor task. , 2001, Brain research. Cognitive brain research.

[4]  S Laureys,et al.  Sleeping brain, learning brain. The role of sleep for memory systems , 2001, Neuroreport.

[5]  M. Merzenich,et al.  Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[7]  Steven Laureys,et al.  Sleep and Motor Skill Learning , 2002, Neuron.

[8]  C. Gilbert,et al.  The Neural Basis of Perceptual Learning , 2001, Neuron.

[9]  R. Poldrack,et al.  Characterizing the neural mechanisms of skill learning and repetition priming: evidence from mirror reading. , 2001, Brain : a journal of neurology.

[10]  A. Karni,et al.  Learning perceptual skills: behavioral probes into adult cortical plasticity , 1997, Current Opinion in Neurobiology.

[11]  J. D. McGaugh.  Memory--a century of consolidation. , 2000, Science.

[12]  K. Doya,et al.  Parallel neural networks for learning sequential procedures , 1999, Trends in Neurosciences.

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

[14]  R. Shadmehr,et al.  Neural correlates of motor memory consolidation. , 1997, Science.

[15]  Kim Kirsner,et al.  Implicit Memory: New Developments , 1993 .

[16]  Michael Gesemann,et al.  Hepatitis B vaccine boosting among young healthy adults , 1995, The Lancet.

[17]  E. Bizzi,et al.  Consolidation in human motor memory , 1996, Nature.

[18]  J. Donoghue,et al.  Plasticity and primary motor cortex. , 2000, Annual review of neuroscience.

[19]  O. Hikosaka,et al.  Characteristics of a long-term procedural skill in the monkey , 1998, Experimental Brain Research.

[20]  Leslie G. Ungerleider,et al.  The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[22]  A. Karni,et al.  The time course of learning a visual skill , 1993, Nature.

[23]  T. Brashers-Krug,et al.  Functional Stages in the Formation of Human Long-Term Motor Memory , 1997, The Journal of Neuroscience.

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

[25]  Leslie G. Ungerleider,et al.  Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning , 2003, Neuropsychologia.

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

[27]  A Karni,et al.  From primed to learn: the saturation of repetition priming and the induction of long-term memory. , 2002, Brain research. Cognitive brain research.

[28]  Avi Karni,et al.  When practice makes perfect , 1995, The Lancet.

[29]  Y. Dudai.  Molecular bases of long-term memories: a question of persistence , 2002, Current Opinion in Neurobiology.

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

[31]  O. Hikosaka,et al.  Learning of sequential movements in the monkey: process of learning and retention of memory. , 1995, Journal of neurophysiology.

[32]  Miya K. Rand,et al.  Characteristics of sequential movements during early learning period in monkeys , 2000, Experimental Brain Research.

[33]  J. Banatvala,et al.  Hepatitis B vaccine boosting among young healthy adults , 1994, The Lancet.

[34]  D. Salmon,et al.  Neurobiology of skill and habit learning , 1995, Current Opinion in Neurobiology.

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

[36]  David A. Caulton,et al.  On the Modularity of Sequence Representation , 1995 .

[37]  A. Karni.  The acquisition of perceptual and motor skills: a memory system in the adult human cortex. , 1996, Brain research. Cognitive brain research.

[38]  R. Passingham,et al.  The Time Course of Changes during Motor Sequence Learning: A Whole-Brain fMRI Study , 1998, NeuroImage.

[39]  U Yinon,et al.  Evidence for long‐term functional plasticity in the visual cortex of adult cats , 1982, The Journal of physiology.

[40]  K. Newell,et al.  Time scales in motor learning and development. , 2001, Psychological review.

[41]  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.

[42]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[43]  A. Gordon,et al.  Functional magnetic resonance imaging of motor, sensory, and posterior parietal cortical areas during performance of sequential typing movements , 1998, Experimental Brain Research.

[44]  Karl J. Friston,et al.  Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  M. Merzenich,et al.  Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.