Differential adaptation of descending motor tracts in musicians

Cerebral Cortex

Volumn 25, Issue 6, 2015, Pages 1490-1498

  Rüber, Theodor ^a,b   Lindenberg, Robert ^a,c   Schlaug, Gottfried ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b UNIVERSITY HOSPITAL BONN   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

diffusion tensor imaging; finger tapping; motor skill; plasticity; white matter

Indexed keywords

ADAPTATION; ADULT; ARTICLE; BRAIN ASYMMETRY; CONTROLLED STUDY; DESCENDING MOTOR TRACT; DIFFUSION TENSOR IMAGING; FEMALE; FINGER TAPPING TEST; FRACTIONAL ANISOTROPY; FUNCTIONAL NEUROIMAGING; GRAY MATTER; HANDEDNESS; HUMAN; HUMAN EXPERIMENT; IMAGE RECONSTRUCTION; INDEX FINGER; KEYBOARD; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; MUSICIAN; NERVE CELL PLASTICITY; NORMAL HUMAN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PYRAMIDAL TRACT; RIGHT HEMISPHERE; VOXEL BASED MORPHOMETRY; WHITE MATTER; ANALYSIS OF VARIANCE; BRAIN; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; MUSIC; PATHOLOGY; PHYSIOLOGY; PROBABILITY; PSYCHOLOGY; PSYCHOMOTOR PERFORMANCE; SENSORY NERVE; STATISTICS; YOUNG ADULT;

ADULT; AFFERENT PATHWAYS; ANALYSIS OF VARIANCE; BRAIN; DIFFUSION TENSOR IMAGING; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MUSIC; PROBABILITY; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL TRACTS; STATISTICS AS TOPIC; YOUNG ADULT;

EID: 84930368915     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht331     Document Type: Article

References (63)

1. Ashe J, Georgopoulos AP. 1994. Movement parameters and neural activity in motor cortex and area 5. Cereb Cortex. 4:590-600.
2. Bangert M, Schlaug G. 2006. Specialization of the specialized in features of external human brain morphology. Eur J Neurosci. 24:1832-1834.
3. Basser PJ. 1995. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 8:333-344.
4. Basser PJ, Mattiello J, LeBihan D. 1994. MR diffusion tensor spectroscopy and imaging. Biophys J. 66:259-267.
5. Beaulieu C. 2002. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 15:435-455.
6. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW. 2007. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? NeuroImage. 34:144-155.
7. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM. 2003. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med. 50:1077-1088.
8. Belhaj-Saif A, Cheney PD. 2000. Plasticity in the distribution of the red nucleus output to forearm muscles after unilateral lesions of the pyramidal tract. J Neurophysiol. 83:3147-3153.
9. Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H, Ullen F. 2005. Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci. 8:1148-1150.
10. Budde MD, Kim JH, Liang HF, Schmidt RE, Russell JH, Cross AH, Song SK. 2007. Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magn Reson Med. 57:688-695.
11. Canedo A. 1997. Primary motor cortex influences on the descending and ascending systems. Prog Neurobiol. 51:287-335.
12. Dale AM, Fischl B, Sereno MI. 1999. Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage. 9:179-194.
13. Dayan E, Cohen LG. 2011. Neuroplasticity subserving motor skill learning. Neuron. 72:443-454.
14. Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E. 1995. Increased cortical representation of the fingers of the left hand in string players. Science. 270:305-307.
15. Engvig A, Fjell AM, Westlye LT, Moberget T, Sundseth O, Larsen VA, Walhovd KB. 2012. Memory training impacts short-term changes in aging white matter: a longitudinal diffusion tensor imaging study. Hum Brain Mapp. 33:2390-2406.
16. Fischl B, Sereno MI, Dale AM. 1999. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuro-Image. 9:195-207.
17. Geyer S, Matelli M, Luppino G, Zilles K. 2000. Functional neuroanatomy of the primate isocortical motor system. Anat Embryol (Berl). 202:443-474.
18. Granziera C, Daducci A, Meskaldji DE, Roche A, Maeder P, Michel P, Hadjikhani N, Sorensen AG, Frackowiak RS, Thiran JP et al. 2012. A new early and automated MRI-based predictor of motor improvement after stroke. Neurology. 79:39-46.
19. Halwani GF, Loui P, Rüber T, Schlaug G. 2011. Effects of practice and experience on the arcuate fasciculus: comparing singers, instrumentalists, and non-musicians. Front Psychol. 2:156.
20. Han Y, Yang H, Lv YT, Zhu CZ, He Y, Tang HH, Gong QY, Luo YJ, Zang YF, Dong Q. 2009. Gray matter density and white matter integrity in pianists' brain: a combined structural and diffusion tensor MRI study. Neurosci Lett. 459:3-6.
21. Hanggi J, Koeneke S, Bezzola L, Jancke L. 2010. Structural neuroplasticity in the sensorimotor network of professional female ballet dancers. Hum Brain Mapp. 31:1196-1206.
22. Heiervang E, Behrens TE, Mackay CE, Robson MD, Johansen-Berg H. 2006. Between session reproducibility and between subject variability of diffusion MR and tractographymeasures. NeuroImage. 33:867-877.
23. Herholz SC, Zatorre RJ. 2012. Musical training as a framework for brain plasticity: behavior, function, and structure. Neuron. 76:486-502.
24. Humphrey DR. 1972. Relating motor cortex spike trains to measures of motor performance. Brain Res. 40:7-18.
25. Hyde KL, Lerch J, Norton A, Forgeard M, Winner E, Evans AC, Schlaug G. 2009. Musical training shapes structural brain development. J Neurosci. 29:3019-3025.
26. Imfeld A, Oechslin MS, Meyer M, Loenneker T, Jancke L. 2009. White matter plasticity in the corticospinal tract of musicians: a diffusion tensor imaging study. NeuroImage. 46:600-607.
27. Jancke L. 2009. The plastic human brain. Restor Neurol Neurosci. 27:521-538.
28. Jancke L, Schlaug G, Steinmetz H. 1997. Hand skill asymmetry in professional musicians. Brain Cogn. 34:424-432.
29. Jenkinson M, Smith S. 2001. A global optimisation method for robust affine registration of brain images. Med Image Anal. 5:143-156.
30. Johansen-Berg H, Scholz J, Stagg CJ. 2010. Relevance of structural brain connectivity to learning and recovery from stroke. Front Syst Neurosci. 4:146.
31. Keil C, Prell T, Peschel T, Hartung V, Dengler R, Grosskreutz J. 2012. Longitudinal diffusion tensor imaging in amyotrophic lateral sclerosis. BMC Neurosci. 13:141.
32. Klawiter EC, Schmidt RE, Trinkaus K, Liang HF, Budde MD, Naismith RT, Song SK, Cross AH, Benzinger TL. 2011. Radial diffusivity predicts demyelination in ex vivo multiple sclerosis spinal cords. NeuroImage. 55:1454-1460.
33. Kopiez R, Galley N, Lehmann AC. 2010. The relation between lateralisation, early start of training, and amount of practice in musicians: a contribution to the problem of handedness classification. Laterality. 15:385-414.
34. Kraus MF, Susmaras T, Caughlin BP, Walker CJ, Sweeney JA, Little DM. 2007. White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain. 130: 2508-2519.
35. Landi SM, Baguear F, Della-Maggiore V. 2011. One week of motor adaptation induces structural changes in primary motor cortex that predict long-term memory one year later. J Neurosci. 31: 11808-11813.
36. Langer N, Hanggi J, Muller NA, Simmen HP, Jancke L. 2012. Effects of limb immobilization on brain plasticity. Neurology. 78:182-188.
37. Lehericy S, Ducros M, Krainik A, Francois C, Van de Moortele PF, Ugurbil K, Kim DS. 2004. 3-D diffusion tensor axonal tracking shows distinct SMA and pre-SMA projections to the human striatum. Cereb Cortex. 14:1302-1309.
38. Lemon RN. 2008. Descending pathways in motor control. Ann Rev Neurosci. 31:195-218.
39. Lindenberg R, Renga V, Zhu LL, Betzler F, Alsop D, Schlaug G. 2010. Structural integrity of corticospinal motor fibers predicts motor impairment in chronic stroke. Neurology. 74:280-287.
40. Lindenberg R, Zhu LL, Rüber T, Schlaug G. 2012. Predicting functional motor potential in chronic stroke patients using diffusion tensor imaging. Hum Brain Mapp. 33:1040-1051.
41. Luo C, Guo ZW, Lai YX, Liao W, Liu Q, Kendrick KM, Yao DZ, Li H. 2012. Musical training induces functional plasticity in perceptual and motor networks: insights from resting-state FMRI. PloS One. 7: e36568.
42. Lutz K, Koeneke S, Wustenberg T, Jancke L. 2005. Asymmetry of cortical activation during maximum and convenient tapping speed. Neurosci Lett. 373:61-66.
43. Milliken GA, Johnson DE. 2009. Analysis of Messy Data, Volume 1: Designed Experiments. Boca Raton (FL): CRC Press.
44. Munte TF, Altenmuller E, Jancke L. 2002. The musician's brain as a model of neuroplasticity. Nat Rev Neurosci. 3:473-478.
45. Nichols TE, Holmes AP. 2002. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp. 15:1-25.
46. Oldfield RC. 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 9:97-113.
47. Pantev C, Roberts LE, Schulz M, Engelien A, Ross B. 2001. Timbrespecific enhancement of auditory cortical representations in musicians. Neuroreport. 12:169-174.
48. Rüber T, Schlaug G, Lindenberg R. 2012. Compensatory role of the cortico-rubro-spinal tract in motor recovery after stroke. Neurology. 79:515-522.
49. Schlaug G. 2001. The brain of musicians. A model for functional and structural adaptation. Ann N Y Acad Sci. 930:281-299.
50. Schlaug G, Forgeard M, Zhu L, Norton A, Norton A, Winner E. 2009. Training-induced neuroplasticity in young children. Ann N Y Acad Sci. 1169:205-208.
51. Schlaug G, Sanes JN, Thangaraj V, Darby DG, Jancke L, Edelman RR, Warach S. 1996. Cerebral activation covaries with movement rate. Neuroreport. 7:879-883.
52. Schmithorst VJ, Wilke M. 2002. Differences in white matter architecture between musicians and non-musicians: a diffusion tensor imaging study. Neurosci Lett. 321:57-60.
53. Scholz J, Klein MC, Behrens TE, Johansen-Berg H. 2009. Training induces changes in white-matter architecture. Nat Neurosci. 12:1370-1371.
54. Smith SM. 2002. Fast robust automated brain extraction. Hum Brain Mapp. 17:143-155.
55. Smith SM, Nichols TE. 2009. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage. 44:83-98.
56. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. 2002. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage. 17:1429-1436.
57. Stewart L. 2008. Do musicians have different brains? Clin Med. 8:304-308.
58. Toosy AT, Werring DJ, Orrell RW, Howard RS, King MD, Barker GJ, Miller DH, Thompson AJ. 2003. Diffusion tensor imaging detects corticospinal tract involvement at multiple levels in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 74: 1250-1257.
59. Westerhausen R, Huster RJ, Kreuder F, Wittling W, Schweiger E. 2007. Corticospinal tract asymmetries at the level of the internal capsule: is there an association with handedness? NeuroImage. 37:379-386.
60. Wheeler-Kingshott CA, Cercignani M. 2009. About "axial" and "radial" diffusivities. Magn Reson Med. 61:1255-1260.
61. Wrigley PJ, Gustin SM, Macey PM, Nash PG, Gandevia SC, Macefield VG, Siddall PJ, Henderson LA. 2009. Anatomical changes in human motor cortex and motor pathways following complete thoracic spinal cord injury. Cerebr Cortex. 19:224-232.
62. Zatorre RJ, Fields RD, Johansen-Berg H. 2012. Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat Neurosci. 15:528-536.
63. Zipse L, Norton A, Marchina S, Schlaug G. 2012. When right is all that is left: plasticity of right-hemisphere tracts in a young aphasic patient. Ann N Y Acad Sci. 1252:237-245.