White matter plasticity in the corticospinal tract of musicians: A diffusion tensor imaging study

With the advent of diffusion tensor imaging (DTI), the study of plastic changes in white matter architecture due to long-term practice has attracted increasing interest. Professional musicians provide an ideal model for investigating white matter plasticity because of their early onset of extensive auditory and sensorimotor training. We performed fiber tractography and subsequent voxelwise analysis, region of interest (ROI) analysis, and detailed slicewise analysis of diffusion parameters in the corticospinal tract (CST) on 26 professional musicians and a control group of 13 participants. All analyses resulted in significantly lower fractional anisotropy (FA) values in both the left and the right CST in the musician group. Furthermore, a right-greater-than-left asymmetry of FA was observed regardless of group. In the musician group, diffusivity was negatively correlated with the onset of musical training in childhood. A subsequent median split into an early and a late onset musician group (median=7 years) revealed increased diffusivity in the CST of the early onset group as compared to both the late onset group and the controls. In conclusion, these DTI-based findings might indicate plastic changes in white matter architecture of the CST in professional musicians. Our results imply that training-induced changes in diffusion characteristics of the axonal membrane may lead to increased radial diffusivity as reflected in decreased FA values.

[1]  Armin Thron,et al.  Cortical activation patterns during complex motor tasks in piano players and control subjects. A functional magnetic resonance imaging study , 2000, Neuroscience Letters.

[2]  S C Gandevia,et al.  Anatomical changes in human motor cortex and motor pathways following complete thoracic spinal cord injury. , 2009, Cerebral cortex.

[3]  Khader M Hasan,et al.  Quantitative diffusion tensor tractography of association and projection fibers in normally developing children and adolescents. , 2007, Cerebral cortex.

[4]  G. Schlaug,et al.  Effects of Music Training on the Child's Brain and Cognitive Development , 2005, Annals of the New York Academy of Sciences.

[5]  R. Oostenveld,et al.  Increased auditory cortical representation in musicians , 1998, Nature.

[6]  S. Mori,et al.  Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research , 2006, Neuron.

[7]  T. Ohnishi,et al.  Functional Anatomy of Musical Perception in Musicians , 2001 .

[8]  Lutz Jäncke,et al.  Enhancement of Auditory-evoked Potentials in Musicians Reflects an Influence of Expertise but not Selective Attention , 2008, Journal of Cognitive Neuroscience.

[9]  L. Jäncke,et al.  Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists. , 2000, Brain research. Cognitive brain research.

[10]  M. Scherg,et al.  Structural and functional asymmetry of lateral Heschl's gyrus reflects pitch perception preference , 2005, Nature Neuroscience.

[11]  I. Peretz,et al.  Brain organization for music processing. , 2005, Annual review of psychology.

[12]  E. Altenmüller,et al.  The musician's brain as a model of neuroplasticity , 2002, Nature Reviews Neuroscience.

[13]  Stefan Skare,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Extensive Blockinpiano Blockinpracticing Blockinhas Blockinregionally Specific Blockineffects Blockinon Blockinwhite Blockinmatter Blockindevelopment , 2022 .

[14]  R. Poldrack,et al.  Microstructure of Temporo-Parietal White Matter as a Basis for Reading Ability Evidence from Diffusion Tensor Magnetic Resonance Imaging , 2000, Neuron.

[15]  M. Annett The Binomial Distribution of Right, Mixed and Left Handedness , 1967, The Quarterly journal of experimental psychology.

[16]  H. Moser,et al.  Imaging cortical association tracts in the human brain using diffusion‐tensor‐based axonal tracking , 2002, Magnetic resonance in medicine.

[17]  Jürgen Hennig,et al.  FiberTools : A Complete Toolbox for DTI Calculation , Fiber Tracking , and Combined Evaluation , 2005 .

[18]  D. Le Bihan,et al.  Diffusion tensor imaging: Concepts and applications , 2001, Journal of magnetic resonance imaging : JMRI.

[19]  R. Kikinis,et al.  Magnetic resonance imaging shows orientation and asymmetry of white matter fiber tracts , 1998, Brain Research.

[20]  M. Moseley Diffusion tensor imaging and aging – a review , 2002, NMR in biomedicine.

[21]  G. Schlaug,et al.  In vivo evidence of structural brain asymmetry in musicians , 1995, Science.

[22]  B. Stankoff,et al.  Induction of myelination in the central nervous system by electrical activity. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Christian Beaulieu,et al.  Diffusion anisotropy in subcortical white matter and cortical gray matter: Changes with aging and the role of CSF‐suppression , 2004, Journal of magnetic resonance imaging : JMRI.

[24]  Khader M. Hasan,et al.  White matter development during late adolescence in healthy males: A cross-sectional diffusion tensor imaging study , 2007, NeuroImage.

[25]  Luis Concha,et al.  Imaging brain connectivity in children with diverse reading ability , 2005, NeuroImage.

[26]  Hangyi Jiang,et al.  DtiStudio: Resource program for diffusion tensor computation and fiber bundle tracking , 2006, Comput. Methods Programs Biomed..

[27]  D. V. von Cramon,et al.  Motor-learning-related changes in piano players and non-musicians revealed by functional magnetic-resonance signals , 1999, Experimental Brain Research.

[28]  V. Schmithorst,et al.  Differences in white matter architecture between musicians and non-musicians: a diffusion tensor imaging study , 2002, Neuroscience Letters.

[29]  Guido Gerig,et al.  Diffusion tensor imaging: Application to the study of the developing brain. , 2007, Journal of the American Academy of Child and Adolescent Psychiatry.

[30]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[31]  A. Alexander,et al.  Diffusion tensor imaging of the brain , 2007, Neurotherapeutics.

[32]  René Westerhausen,et al.  Corticospinal tract asymmetries at the level of the internal capsule: Is there an association with handedness? , 2007, NeuroImage.

[33]  D. Reich,et al.  Quantitative characterization of the corticospinal tract at 3T. , 2006, AJNR. American journal of neuroradiology.

[34]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[35]  G. Schlaug,et al.  Cerebellar volume of musicians. , 2003, Cerebral cortex.

[36]  Bruce D. McCandliss,et al.  Left lateralized white matter microstructure accounts for individual differences in reading ability and disability , 2006, Neuropsychologia.

[37]  Christian Gaser,et al.  Differ between Musicians and NonMusicians , 2003 .

[38]  Christian Beaulieu,et al.  Voxel based versus region of interest analysis in diffusion tensor imaging of neurodevelopment , 2007, NeuroImage.

[39]  Brian T. Gold,et al.  Speed of lexical decision correlates with diffusion anisotropy in left parietal and frontal white matter: Evidence from diffusion tensor imaging , 2007, Neuropsychologia.

[40]  P. Sundgren,et al.  Diffusion tensor imaging of the brain: review of clinical applications , 2004, Neuroradiology.

[41]  M. Bangert,et al.  Mapping perception to action in piano practice: a longitudinal DC-EEG study , 2003, BMC Neuroscience.

[42]  Thomas R. Barrick,et al.  Voxel-Based Morphometry Reveals Increased Gray Matter Density in Broca's Area in Male Symphony Orchestra Musicians , 2002, NeuroImage.

[43]  T. Ohnishi,et al.  Functional anatomy of musical perception in musicians , 2001, NeuroImage.

[44]  G. Schlaug The Brain of Musicians , 2001, Annals of the New York Academy of Sciences.

[45]  J. Staiger,et al.  Increased corpus callosum size in musicians , 1995, Neuropsychologia.

[46]  J. Sweeney,et al.  White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. , 2007, Brain : a journal of neurology.

[47]  C. Büchel,et al.  White matter asymmetry in the human brain: a diffusion tensor MRI study. , 2004, Cerebral cortex.

[48]  B. Rockstroh,et al.  Increased Cortical Representation of the Fingers of the Left Hand in String Players , 1995, Science.

[49]  G. Schlaug,et al.  Absolute Pitch and Planum Temporale , 2001, NeuroImage.

[50]  E. Syková,et al.  Evolution of anisotropic diffusion in the developing rat corpus callosum. , 1997, Journal of neurophysiology.

[51]  G J Barker,et al.  Diffusion tensor imaging detects corticospinal tract involvement at multiple levels in amyotrophic lateral sclerosis , 2003, Journal of neurology, neurosurgery, and psychiatry.

[52]  Armin Thron,et al.  Effects of long‐term practice and task complexity in musicians and nonmusicians performing simple and complex motor tasks: Implications for cortical motor organization , 2005, Human brain mapping.