Repetitive transcranial magnetic stimulation over the primary motor cortex disrupts early boost but not delayed gains in performance in motor sequence learning

In humans the consolidation of recently learned motor skills is a multi‐step process. We previously showed that performance on the finger‐tapping task (FTT; i.e. a sequential motor skill) temporarily improves early on, 5–30 min after practice has ended, but not 4 h later. In the absence of any further practice to the task, this early boost in performance was predictive of the performance levels eventually achieved 48 h later, suggesting its functional relevance for long‐term memory consolidation [ Hotermans, Peigneux, Maertens de Noordhout, Moonen, and Maquet (2006) Early boost and slow consolidation in motor skill learning. Learn. Mem., 13, 580–583]. Here, we focused on the role of the primary motor cortex (M1) in consolidation using repetitive transcranial magnetic stimulation (rTMS) applied immediately before testing at 30 min, 4 or 24 h after practice of the FTT. Immediately after learning, rTMS over M1 depressed the early boost in performance, but did not affect the delayed improvement observed 48 h later. Four and 24 h after practice, rTMS did not disrupt performance anymore. These results suggest that M1 supports performance during the early post‐training phase of motor skill consolidation, but is no longer mandatory in the subsequent, delayed stages of consolidation.

[1]  James L. McClelland,et al.  Learning the structure of event sequences. , 1991, Journal of experimental psychology. General.

[2]  S. Boniface,et al.  Magnetic brain stimulation with a double coil: the importance of coil orientation. , 1992, Electroencephalography and clinical neurophysiology.

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

[4]  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.

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

[6]  J. Kleim,et al.  Functional reorganization of the rat motor cortex following motor skill learning. , 1998, Journal of neurophysiology.

[7]  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.

[8]  K. Svoboda,et al.  Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. , 1999, Science.

[9]  K. Svoboda,et al.  Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. , 1999, Science.

[10]  T Seidenbecher,et al.  Reinforcement of Early Long-Term Potentiation (Early-LTP) in Dentate Gyrus by Stimulation of the Basolateral Amygdala: Heterosynaptic Induction Mechanisms of Late-LTP , 2001, The Journal of Neuroscience.

[11]  J. Pine,et al.  Chunking mechanisms in human learning , 2001, Trends in Cognitive Sciences.

[12]  M. Hallett,et al.  Early consolidation in human primary motor cortex , 2002, Nature.

[13]  J. Doyon,et al.  Dynamic Cortical and Subcortical Networks in Learning and Delayed Recall of Timed Motor Sequences , 2002, The Journal of Neuroscience.

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

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

[16]  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.

[17]  Karl J. Friston,et al.  Acute Remapping within the Motor System Induced by Low-Frequency Repetitive Transcranial Magnetic Stimulation , 2003, The Journal of Neuroscience.

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

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

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

[21]  O. Hikosaka,et al.  Chunking during human visuomotor sequence learning , 2003, Experimental Brain Research.

[22]  J. Kleim,et al.  Cortical Synaptogenesis and Motor Map Reorganization Occur during Late, But Not Early, Phase of Motor Skill Learning , 2004, The Journal of Neuroscience.

[23]  D. Wolpert,et al.  Consolidation of Dynamic Motor Learning Is Not Disrupted by rTMS of Primary Motor Cortex , 2004, Current Biology.

[24]  M. Nicolelis,et al.  Differential Corticostriatal Plasticity during Fast and Slow Motor Skill Learning in Mice , 2004, Current Biology.

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

[26]  Yoram Ben-Shaul,et al.  Neuronal activity in motor cortical areas reflects the sequential context of movement. , 2004, Journal of neurophysiology.

[27]  J. Doyon,et al.  Reorganization and plasticity in the adult brain during learning of motor skills , 2005, Current Opinion in Neurobiology.

[28]  J. Doyon,et al.  Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[31]  P. Matthews,et al.  Distinguishable brain activation networks for short- and long-term motor skill learning. , 2005, Journal of neurophysiology.

[32]  J. Ashe,et al.  Anticipatory Activity in Primary Motor Cortex Codes Memorized Movement Sequences , 2005, Neuron.

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

[34]  Alexandra T Basford,et al.  Cortical control of motor sequences , 2006, Current Opinion in Neurobiology.

[35]  U. Halsband,et al.  Motor learning in man: A review of functional and clinical studies , 2006, Journal of Physiology-Paris.

[36]  C. Degueldre,et al.  Offline Persistence of Memory-Related Cerebral Activity during Active Wakefulness , 2006, PLoS biology.

[37]  Emilio Bizzi,et al.  Disruption of Primary Motor Cortex before Learning Impairs Memory of Movement Dynamics , 2006, The Journal of Neuroscience.

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

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

[40]  A. Luft,et al.  Stages of motor skill learning , 2005, Molecular Neurobiology.