Skill learning strengthens cortical representations of motor sequences

Motor-skill learning can be accompanied by both increases and decreases in brain activity. Increases may indicate neural recruitment, while decreases may imply that a region became unimportant or developed a more efficient representation of the skill. These overlapping mechanisms make interpreting learning-related changes of spatially averaged activity difficult. Here we show that motor-skill acquisition is associated with the emergence of highly distinguishable activity patterns for trained movement sequences, in the absence of average activity increases. During functional magnetic resonance imaging, participants produced either four trained or four untrained finger sequences. Using multivariate pattern analysis, both untrained and trained sequences could be discriminated in primary and secondary motor areas. However, trained sequences were classified more reliably, especially in the supplementary motor area. Our results indicate skill learning leads to the development of specialized neuronal circuits, which allow the execution of fast and accurate sequential movements without average increases in brain activity. DOI: http://dx.doi.org/10.7554/eLife.00801.001

[1]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[2]  V. Penhune,et al.  Specific Increases within Global Decreases: A Functional Magnetic Resonance Imaging Investigation of Five Days of Motor Sequence Learning , 2010, The Journal of Neuroscience.

[3]  Qi Zhu,et al.  Motor Training Increases the Stability of Activation Patterns in the Primary Motor Cortex , 2013, PloS one.

[4]  Simon B. Eickhoff,et al.  The Role of Human Parietal Area 7A as a Link between Sequencing in Hand Actions and in Overt Speech Production , 2012, Front. Psychology.

[5]  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.

[6]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[7]  P. Strick,et al.  Skill representation in the primary motor cortex after long-term practice. , 2007, Journal of neurophysiology.

[8]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[9]  David G. Stork,et al.  Pattern Classification , 1973 .

[10]  M. Hallett,et al.  How self-initiated memorized movements become automatic: a functional MRI study. , 2004, Journal of neurophysiology.

[11]  Sabrina M. Tom,et al.  The Neural Correlates of Motor Skill Automaticity , 2005, The Journal of Neuroscience.

[12]  Shigeo Abe DrEng Pattern Classification , 2001, Springer London.

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

[14]  Jörn Diedrichsen,et al.  Interaction of temporal and ordinal representations in movement sequences. , 2013, Journal of neurophysiology.

[15]  Julien Doyon,et al.  Cerebellum and M1 interaction during early learning of timed motor sequences , 2005, NeuroImage.

[16]  Katrin Amunts,et al.  Cortical Folding Patterns and Predicting Cytoarchitecture , 2007, Cerebral cortex.

[17]  Jörn Diedrichsen,et al.  A multivariate method to determine the dimensionality of neural representation from population activity , 2013, NeuroImage.

[18]  J. Tanji,et al.  Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. , 1998, Journal of neurophysiology.

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

[20]  John Duncan,et al.  Hierarchical Organization of Cognition Reflected in Distributed Frontoparietal Activity , 2012, The Journal of Neuroscience.

[21]  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.

[22]  L. Cohen,et al.  Neuroplasticity Subserving Motor Skill Learning , 2011, Neuron.

[23]  Karl J. Friston,et al.  Comparing the similarity and spatial structure of neural representations: A pattern-component model , 2011, NeuroImage.

[24]  Jun Tanji,et al.  Role for supplementary motor area cells in planning several movements ahead , 1994, Nature.

[25]  Karl J. Friston,et al.  Recognizing Sequences of Sequences , 2009, PLoS Comput. Biol..

[26]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

[27]  Gary F. Egan,et al.  Long-term motor training induced changes in regional cerebral blood flow in both task and resting states , 2009, NeuroImage.

[28]  Paul E. Downing,et al.  A comparison of volume-based and surface-based multi-voxel pattern analysis , 2011, NeuroImage.

[29]  R. Poldrack Imaging Brain Plasticity: Conceptual and Methodological Issues— A Theoretical Review , 2000, NeuroImage.

[30]  D. Brooks,et al.  Motor sequence learning: a study with positron emission tomography , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Jeremy Freeman,et al.  Orientation Decoding Depends on Maps, Not Columns , 2011, The Journal of Neuroscience.

[32]  Kenneth F. Valyear,et al.  Human parietal cortex in action , 2006, Current Opinion in Neurobiology.

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

[34]  Robert Turner,et al.  Image Distortion Correction in fMRI: A Quantitative Evaluation , 2002, NeuroImage.

[35]  Hartwig R. Siebner,et al.  Increased Facilitatory Connectivity from the Pre-SMA to the Left Dorsal Premotor Cortex during Pseudoword Repetition , 2013, Journal of Cognitive Neuroscience.

[36]  M. Rushworth,et al.  Organization of action sequences and the role of the pre-SMA. , 2004, Journal of neurophysiology.

[37]  Simon B. Eickhoff,et al.  A quantitative meta-analysis and review of motor learning in the human brain , 2013, NeuroImage.

[38]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[39]  J Randall Flanagan,et al.  Where One Hand Meets the Other: Limb-Specific and Action-Dependent Movement Plans Decoded from Preparatory Signals in Single Human Frontoparietal Brain Areas , 2013, The Journal of Neuroscience.

[40]  Jörn Diedrichsen,et al.  Two Distinct Ipsilateral Cortical Representations for Individuated Finger Movements , 2012, Cerebral cortex.

[41]  Jascha D. Swisher,et al.  Multiscale Pattern Analysis of Orientation-Selective Activity in the Primary Visual Cortex , 2010, The Journal of Neuroscience.

[42]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[43]  Scott T. Grafton,et al.  Functional Mapping of Sequence Learning in Normal Humans , 1995, Journal of Cognitive Neuroscience.

[44]  Peter T. Fox,et al.  Changes in regional activity are accompanied with changes in inter-regional connectivity during 4 weeks motor learning , 2010, Brain Research.

[45]  Jörn Diedrichsen,et al.  Detecting and adjusting for artifacts in fMRI time series data , 2005, NeuroImage.

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

[47]  Scott T. Grafton,et al.  Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study. , 1997, Brain : a journal of neurology.

[48]  M Hallett,et al.  Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. , 1997, Brain : a journal of neurology.

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

[50]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[51]  V. Penhune,et al.  Author's Personal Copy Behavioural Brain Research Parallel Contributions of Cerebellar, Striatal and M1 Mechanisms to Motor Sequence Learning , 2022 .

[52]  Leslie G. Ungerleider,et al.  Imaging Brain Plasticity during Motor Skill Learning , 2002, Neurobiology of Learning and Memory.

[53]  Kathleen A. Hansen,et al.  Modeling low‐frequency fluctuation and hemodynamic response timecourse in event‐related fMRI , 2008, Human brain mapping.