Short‐term plasticity following motor sequence learning revealed by diffusion magnetic resonance imaging

Current noninvasive methods to detect structural plasticity in humans are mainly used to study long‐term changes. Diffusion magnetic resonance imaging (MRI) was recently proposed as a novel approach to reveal gray matter changes following spatial navigation learning and object‐location memory tasks. In the present work, we used diffusion MRI to investigate the short‐term neuroplasticity that accompanies motor sequence learning. Following a 45‐min training session in which participants learned to accurately play a short sequence on a piano keyboard, changes in diffusion properties were revealed mainly in motor system regions such as the premotor cortex and cerebellum. In a second learning session taking place immediately afterward, feedback was given on the timing of key pressing instead of accuracy, while participants continued to learn. This second session induced a different plasticity pattern, demonstrating the dynamic nature of learning‐induced plasticity, formerly thought to require months of training in order to be detectable. These results provide us with an important reminder that the brain is an extremely dynamic structure. Furthermore, diffusion MRI offers a novel measure to follow tissue plasticity particularly over short timescales, allowing new insights into the dynamics of structural brain plasticity.

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

[2]  J. Diedrichsen,et al.  Motor skill learning between selection and execution , 2015, Trends in Cognitive Sciences.

[3]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.

[4]  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.

[5]  Rainer Goebel,et al.  Continuous motor sequence learning: Cortical efficiency gains accompanied by striatal functional reorganization , 2010, NeuroImage.

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

[7]  P. Janata,et al.  Activation of the inferior frontal cortex in musical priming. , 2003, Annals of the New York Academy of Sciences.

[8]  S. Killcross,et al.  Inactivation of the infralimbic prefrontal cortex reinstates goal-directed responding in overtrained rats , 2003, Behavioural Brain Research.

[9]  Hans-Jochen Heinze,et al.  Shared networks for auditory and motor processing in professional pianists: Evidence from fMRI conjunction , 2006, NeuroImage.

[10]  Yaniv Assaf,et al.  The rapid development of structural plasticity through short water maze training: A DTI study , 2017, NeuroImage.

[11]  J. Doyon,et al.  Contributions of the basal ganglia and functionally related brain structures to motor learning , 2009, Behavioural Brain Research.

[12]  Luca Cocchi,et al.  Brain changes following four weeks of unimanual motor training: Evidence from behavior, neural stimulation, cortical thickness, and functional MRI , 2017, Human brain mapping.

[13]  E. Zimmerman,et al.  The multisensory brain and its ability to learn music , 2012, Annals of the New York Academy of Sciences.

[14]  Scott K. Holland,et al.  The effect of musical training on music processing: a functional magnetic resonance imaging study in humans , 2003, Neuroscience Letters.

[15]  Habib Benali,et al.  Dynamics of motor-related functional integration during motor sequence learning , 2010, NeuroImage.

[16]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

[17]  Christo Pantev,et al.  Dissociation of Neural Networks for Predisposition and for Training-Related Plasticity in Auditory-Motor Learning. , 2016, Cerebral cortex.

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

[19]  Y. Assaf,et al.  Diffusion MRI of Structural Brain Plasticity Induced by a Learning and Memory Task , 2011, PloS one.

[20]  Hans Knutsson,et al.  Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates , 2016, Proceedings of the National Academy of Sciences.

[21]  Chris I. Baker,et al.  Teaching an adult brain new tricks: A critical review of evidence for training-dependent structural plasticity in humans , 2013, NeuroImage.

[22]  Timothy Edward John Behrens,et al.  Training induces changes in white matter architecture , 2009, Nature Neuroscience.

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

[24]  Justine Sergent,et al.  The brain basis of piano performance , 2005, Neuropsychologia.

[25]  Nancy Kanwisher,et al.  Sensitivity to musical structure in the human brain. , 2012, Journal of neurophysiology.

[26]  Yaniv Assaf,et al.  Short-Term Learning Induces White Matter Plasticity in the Fornix , 2013, The Journal of Neuroscience.

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

[28]  Takamitsu Watanabe,et al.  Memory of music: Roles of right hippocampus and left inferior frontal gyrus , 2008, NeuroImage.

[29]  K. Wadden,et al.  Motor skill acquisition across short and long time scales: A meta-analysis of neuroimaging data , 2014, Neuropsychologia.

[30]  Yaniv Assaf New dimensions for brain mapping , 2018, Science.

[31]  Hans Forssberg,et al.  Listening to rhythms activates motor and premotor cortices , 2009, Cortex.

[32]  Ching-I Lu The effect of musical training on verbal and tonal working memory , 2012 .

[33]  A. Salmoni Motor skill learning. , 1989 .

[34]  Yaniv Assaf,et al.  Micro-structural assessment of short term plasticity dynamics , 2013, NeuroImage.

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

[36]  Nobuko Kemmotsu,et al.  Functional MRI of motor sequence acquisition: effects of learning stage and performance. , 2002, Brain research. Cognitive brain research.

[37]  G. Schlaug,et al.  Brain Structures Differ between Musicians and Non-Musicians , 2003, The Journal of Neuroscience.

[38]  Benjamin O. Turner,et al.  Cortical and basal ganglia contributions to habit learning and automaticity , 2010, Trends in Cognitive Sciences.

[39]  E. Saltzman,et al.  Action Representation of Sound: Audiomotor Recognition Network While Listening to Newly Acquired Actions , 2007, The Journal of Neuroscience.

[40]  Anatol C. Kreitzer,et al.  Plasticity in gray and white: neuroimaging changes in brain structure during learning , 2012, Nature Neuroscience.

[41]  A. Chun,et al.  On the brain , 2007, Nature Nanotechnology.

[42]  Yaniv Assaf,et al.  Learning in the Fast Lane: New Insights into Neuroplasticity , 2012, Neuron.

[43]  Lutz Jäncke,et al.  Training-Induced Neural Plasticity in Golf Novices , 2011, The Journal of Neuroscience.

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

[45]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[46]  K. Doya Complementary roles of basal ganglia and cerebellum in learning and motor control , 2000, Current Opinion in Neurobiology.

[47]  David L Wright,et al.  A cognitive framework for explaining serial processing and sequence execution strategies , 2015, Psychonomic bulletin & review.

[48]  Heidi Johansen-Berg,et al.  Fornix Microstructure Correlates with Recollection But Not Familiarity Memory , 2009, The Journal of Neuroscience.

[49]  J. Doyon,et al.  Current issues related to motor sequence learning in humans , 2018, Current Opinion in Behavioral Sciences.

[50]  M. Erb,et al.  Fast track to the neocortex: A memory engram in the posterior parietal cortex , 2018, Science.

[51]  Kate E. Watkins,et al.  Learning to play a melody: An fMRI study examining the formation of auditory-motor associations , 2012, NeuroImage.

[52]  Robert J Zatorre,et al.  Neural network retuning and neural predictors of learning success associated with cello training , 2018, Proceedings of the National Academy of Sciences.

[53]  A. Dickinson,et al.  Differential Engagement of the Ventromedial Prefrontal Cortex by Goal-Directed and Habitual Behavior toward Food Pictures in Humans , 2009, The Journal of Neuroscience.

[54]  M. Hallett,et al.  Role of the human motor cortex in rapid motor learning , 2001, Experimental Brain Research.

[55]  Robert J. Zatorre,et al.  Musical Training as a Framework for Brain Plasticity: Behavior, Function, and Structure , 2012, Neuron.

[56]  Michael B. Miller,et al.  The principled control of false positives in neuroimaging. , 2009, Social cognitive and affective neuroscience.

[57]  Kae Nakamura,et al.  Central mechanisms of motor skill learning , 2002, Current Opinion in Neurobiology.

[58]  Heidi Johansen-Berg,et al.  Human Structural Plasticity at Record Speed , 2012, Neuron.

[59]  Adam G. Thomas,et al.  Functional but not structural changes associated with learning: An exploration of longitudinal Voxel-Based Morphometry (VBM) , 2009, NeuroImage.

[60]  C. Zou,et al.  Diurnal Microstructural Variations in Healthy Adult Brain Revealed by Diffusion Tensor Imaging , 2014, PloS one.

[61]  M. Delgado,et al.  Modulation of Caudate Activity by Action Contingency , 2004, Neuron.

[62]  Marc Leman,et al.  The Cortical Topography of Tonal Structures Underlying Western Music , 2002, Science.

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

[64]  Bogdan Draganski,et al.  Neuroplasticity: Changes in grey matter induced by training , 2004, Nature.