White matter microstructure changes induced by motor skill learning utilizing a body machine interface

NeuroImage

Volumn 88, Issue , 2014, Pages 32-40

  Wang, Xue ^a   Casadio, Maura ^b,c   Weber, Kenneth A ^d   Mussa Ivaldi, Ferdinando A ^a,b,e   Parrish, Todd B ^a,d,e  

^a NORTHWESTERN UNIVERSITY   (United States)

^b REHABILITATION INSTITUTE OF CHICAGO   (United States)

^c UNIVERSITY OF GENOA   (Italy)

^d NORTHWESTERN UNIVERSITY   (United States)

^e Northwestern University   (United States)

Author keywords

Diffusion tensor imaging; Fractional anisotropy; Motor skill learning; White matter plasticity

Indexed keywords

MYELIN;

ADULT; ARM MOVEMENT; ARTICLE; BODY MACHINE INTERFACE; BODY MOVEMENT; CAPSULA INTERNA; COMPUTER INTERFACE; CORPUS CALLOSUM; DEPTH PERCEPTION; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NERVE FIBER; NORMAL HUMAN; PRIORITY JOURNAL; TASK PERFORMANCE; VISUAL FEEDBACK; VOLUNTEER; WHITE MATTER; YOUNG ADULT; ANATOMY AND HISTOLOGY; DIAGNOSTIC IMAGING; MOTOR ACTIVITY; PHYSIOLOGY; PROCEDURES; VISION;

ADULT; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; INTERNAL CAPSULE; LEARNING; MALE; MOTOR ACTIVITY; MOTOR SKILLS; NEURONAL PLASTICITY; SPACE PERCEPTION; VISUAL PERCEPTION; WHITE MATTER; YOUNG ADULT;

EID: 84892839482     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.10.066     Document Type: Article

References (68)

1. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 1986, 9:357-381.
2. Andersson J.L.R., Jenkinson M., Smith S. Non-linear optimisation. FMRIB Technical Report TR07JA1 2007, (from www.fmrib.ox.ac.uk/analysis/techrep).
3. Andersson J.L.R., Jenkinson M., Smith S. Non-linear registration, aka spatial normalisation. FMRIB Technical Report TR07JA2 2007, (from www.fmrib.ox.ac.uk/analysis/techrep).
4. Basser P.J., Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 1996, 111:209-219.
5. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002, 15:435-455.
6. Beaulieu C. The biological basis of diffusion anistropy. Diffusion MRI: From Quantitative Measurement to In-vivo Neuroanatomy 2009, Elsevier/Academic Press, Amsterdam. H. Johansen-Berg, T.E.J. Behrens (Eds.).
7. Behrens T.E., Berg H.J., Jbabdi S., Rushworth M.F., Woolrich M.W. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain?. Neuroimage 2007, 34:144-155.
8. Bengtsson S.L., Nagy Z., Skare S., Forsman L., Forssberg H., Ullen F. Extensive piano practicing has regionally specific effects on white matter development. Nat. Neurosci. 2005, 8:1148-1150.
9. Bermudez P., Zatorre R.J. Differences in gray matter between musicians and nonmusicians. Ann. N. Y. Acad. Sci. 2005, 1060:395-399.
10. Blumenfeld-Katzir T., Pasternak O., Dagan M., Assaf Y. Diffusion MRI of structural brain plasticity induced by a learning and memory task. PLoS One 2011, 6:e20678.
11. Bonzano L., Tacchino A., Roccatagliata L., Abbruzzese G., Mancardi G.L., Bove M. Callosal contributions to simultaneous bimanual finger movements. J. Neurosci. 2008, 28:3227-3233.
12. Boyke J., Driemeyer J., Gaser C., Buchel C., May A. Training-induced brain structure changes in the elderly. J. Neurosci. 2008, 28:7031-7035.
13. Cannonieri G.C., Bonilha L., Fernandes P.T., Cendes F., Li L.M. Practice and perfect: length of training and structural brain changes in experienced typists. Neuroreport 2007, 18:1063-1066.
14. Casadio M., Pressman A., Fishbach A., Danziger Z., Acosta S., Chen D., Tseng H.Y., Mussa-Ivaldi F.A. Functional reorganization of upper-body movement after spinal cord injury. Exp. Brain Res. 2010, 207:233-247.
15. Casadio M., Ranganathan R., Mussa-Ivaldi F.A. The body-machine interface: a new perspective on an old theme. J. Mot. Behav. 2012, 44:419-433.
16. Danziger Z., Mussa-Ivaldi F.A. The influence of visual motion on motor learning. J. Neurosci. 2012, 32:9859-9869.
17. Davidson P.R., Wolpert D.M. Motor learning and prediction in a variable environment. Curr. Opin. Neurobiol. 2003, 13:232-237.
18. Dayan E., Cohen L.G. Neuroplasticity subserving motor skill learning. Neuron 2011, 72:443-454.
19. Draganski B., Kherif F. In vivo assessment of use-dependent brain plasticity-beyond the "one trick pony" imaging strategy. Neuroimage 2013, 73:255-259. (discussion 265-257).
20. Draganski B., Gaser C., Busch V., Schuierer G., Bogdahn U., May A. Neuroplasticity: changes in grey matter induced by training. Nature 2004, 427:311-312.
21. Driemeyer J., Boyke J., Gaser C., Buchel C., May A. Changes in gray matter induced by learning-revisited. PLoS One 2008, 3:e2669.
22. Dudai Y. The Neurobiology of Memory: Concepts, Findings, Trends 1989, Oxford University Press, USA.
23. Erickson K.I. Evidence for structural plasticity in humans: comment on Thomas and Baker (2012). Neuroimage 2013, 73:237-238. (discussion 265-237).
24. Fields R.D. White matter in learning, cognition and psychiatric disorders. Trends Neurosci. 2008, 31:361-370.
25. Fields R.D. Imaging learning: the search for a memory trace. Neuroscientist 2011, 17:185-196.
26. Fields R.D. Changes in brain structure during learning: fact or artifact? Reply to Thomas and Baker. Neuroimage 2013, 73:260-264. (discussion 265-267).
27. Freund P., Weiskopf N., Ward N.S., Hutton C., Gall A., Ciccarelli O., Craggs M., Friston K., Thompson A.J. Disability, atrophy and cortical reorganization following spinal cord injury. Brain 2011, 134:1610-1622.
28. Gaser C., Schlaug G. Brain structures differ between musicians and non-musicians. J. Neurosci. 2003, 23:9240-9245.
29. Gulani V., Webb A.G., Duncan I.D., Lauterbur P.C. Apparent diffusion tensor measurements in myelin-deficient rat spinal cords. Magn. Reson. Med. 2001, 45:191-195.
30. Han Y., Yang H., Lv Y.T., Zhu C.Z., He Y., Tang H.H., Gong Q.Y., Luo Y.J., Zang Y.F., Dong Q. Gray matter density and white matter integrity in pianists' brain: a combined structural and diffusion tensor MRI study. Neurosci. Lett. 2009, 459:3-6.
31. Hardwick R.M., Rottschy C., Miall R.C., Eickhoff S.B. A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 2013, 67:283-297.
32. Harsan L.A., Poulet P., Guignard B., Parizel N., Skoff R.P., Ghandour M.S. Astrocytic hypertrophy in dysmyelination influences the diffusion anisotropy of white matter. J. Neurosci. Res. 2007, 85:935-944.
33. Hebb D.O. Organization of Behavior 1949, Wiley and Sons, New York.
34. Henderson L.A., Gustin S.M., Macey P.M., Wrigley P.J., Siddall P.J. Functional reorganization of the brain in humans following spinal cord injury: evidence for underlying changes in cortical anatomy. J. Neurosci. 2011, 31:2630-2637.
35. Hofer S., Frahm J. Topography of the human corpus callosum revisited-comprehensive fiber tractography using diffusion tensor magnetic resonance imaging. Neuroimage 2006, 32:989-994.
36. Hua K., Zhang J., Wakana S., Jiang H., Li X., Reich D.S., Calabresi P.A., Pekar J.J., van Zijl P.C., Mori S. Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. Neuroimage 2008, 39:336-347.
37. Imfeld A., Oechslin M.S., Meyer M., Loenneker T., Jancke L. White matter plasticity in the corticospinal tract of musicians: a diffusion tensor imaging study. Neuroimage 2009, 46:600-607.
38. Jancke L., Koeneke S., Hoppe A., Rominger C., Hanggi J. The architecture of the golfer's brain. PLoS One 2009, 4:e4785.
39. Jenkinson M., Beckmann C.F., Behrens T.E., Woolrich M.W., Smith S.M. FSL. NeuroImage 2012, 62:782-790.
40. Johansen-Berg H., Behrens T.E. Diffusion MRI: From Quantitative Measurement to In-vivo Neuroanatomy 2009, Academic Press.
41. Jolliffe I.T. Principal Component Analysis 2002, Springer, New York, NY.
42. Jung R.E., Caprihan A., Chavez R.S., Flores R.A., Sharrar J., Qualls C.R., Sibbitt W., Roldan C.A. Diffusion tensor imaging in neuropsychiatric systemic lupus erythematosus. BMC Neurol. 2010, 10:65.
43. Kandel E.R., Schwartz J.H., Jessell T.M., Siegebaum S.A., Hudspeth A.J. Principles of Neural Science 2012, McGraw Hill Medical. Fifth edition.
44. Kantak S.S., Winstein C.J. Learning-performance distinction and memory processes for motor skills: a focused review and perspective. Behav. Brain Res. 2012, 228:219-231.
45. Landi S.M., Baguear F., Della-Maggiore V. One week of motor adaptation induces structural changes in primary motor cortex that predict long-term memory one year later. J. Neurosci. 2011, 31:11808-11813.
46. Lee M.R., Gallen C.L., Ross T.J., Kurup P., Salmeron B.J., Hodgkinson C.A., Goldman D., Stein E.A., Enoch M.A. A preliminary study suggests that nicotine and prefrontal dopamine affect cortico-striatal areas in smokers with performance feedback. Genes Brain Behav. 2013, 12:554-563.
47. Lehéricy S., Ducros M., Van De Moortele P.-F., Francois C., Thivard L., Poupon C., Swindale N., Ugurbil K., Kim D.-S. Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans. Ann. Neurol. 2004, 55:522-529.
48. Maguire E.A., Gadian D.G., Johnsrude I.S., Good C.D., Ashburner J., Frackowiak R.S., Frith C.D. Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4398-4403.
49. Monnig M.A., Caprihan A., Yeo R.A., Gasparovic C., Ruhl D.A., Lysne P., Bogenschutz M.P., Hutchison K.E., Thoma R.J. Diffusion tensor imaging of white matter networks in individuals with current and remitted alcohol use disorders and comorbid conditions. Psychol. Addict. Behav. 2013, 27:455-465.
50. Ono J., Harada K., Takahashi M., Maeda M., Ikenaka K., Sakurai K., Sakai N., Kagawa T., Fritz-Zieroth B., Nagai T., et al. Differentiation between dysmyelination and demyelination using magnetic resonance diffusional anisotropy. Brain Res. 1995, 671:141-148.
51. Ostry D.J., Darainy M., Mattar A.A., Wong J., Gribble P.L. Somatosensory plasticity and motor learning. J. Neurosci. 2010, 30:5384-5393.
52. Park I.S., Lee K.J., Han J.W., Lee N.J., Lee W.T., Park K.A., Rhyu I.J. Experience-dependent plasticity of cerebellar vermis in basketball players. Cerebellum 2009, 8:334-339.
53. Reich D.S., Smith S.A., Jones C.K., Zackowski K.M., van Zijl P.C., Calabresi P.A., Mori S. Quantitative characterization of the corticospinal tract at 3T. AJNR Am. J. Neuroradiol. 2006, 27:2168-2178.
54. Scholz J., Klein M.C., Behrens T.E., Johansen-Berg H. Training induces changes in white-matter architecture. Nat. Neurosci. 2009, 12:1370-1371.
55. Shadmehr R., Mussa-Ivaldi F.A. Adaptive representation of dynamics during learning of a motor task. J. Neurosci. 1994, 14:3208-3224.
56. Shmuelof L., Krakauer J.W. Are we ready for a natural history of motor learning?. Neuron 2011, 72(3):469-476.
57. Smith S.M., Jenkinson M., Johansen-Berg H., Rueckert D., Nichols T.E., Mackay C.E., Watkins K.E., Ciccarelli O., Cader M.Z., Matthews P.M., Behrens T.E. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006, 31:1487-1505.
58. Song S.K., Sun S.W., Ramsbottom M.J., Chang C., Russell J., Cross A.H. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 2002, 17:1429-1436.
59. Taubert M., Draganski B., Anwander A., Muller K., Horstmann A., Villringer A., Ragert P. Dynamic properties of human brain structure: learning-related changes in cortical areas and associated fiber connections. J. Neurosci. 2010, 30:11670-11677.
60. Teulings H.L., Contreras-Vidal J.L., Stelmach G.E., Adler C.H. Parkinsonism reduces coordination of fingers, wrist, and arm in fine motor control. Exp. Neurol. 1997, 146:159-170.
61. Thomas C., Baker C.I. On evidence, biases and confounding factors: response to commentaries. Neuroimage 2013, 73:265-267.
62. Thomas C., Baker C.I. Teaching an adult brain new tricks: a critical review of evidence for training-dependent structural plasticity in humans. Neuroimage 2013, 73:225-236.
63. Ungerleider L.G., Doyon J., Karni A. Imaging brain plasticity during motor skill learning. Neurobiol. Learn. Mem. 2002, 78:553-564.
64. Westerhausen R., Huster R.J., Kreuder F., Wittling W., Schweiger E. Corticospinal tract asymmetries at the level of the internal capsule: is there an association with handedness?. Neuroimage 2007, 37:379-386.
65. Wolpert D.M., Miall R.C., Kawato M. Internal models in the cerebellum. Trends Cogn. Sci. 1998, 2:338-347.
66. Zarei M., Johansen-Berg H., Jenkinson M., Ciccarelli O., Thompson A.J., Matthews P.M. Two-dimensional population map of cortical connections in the human internal capsule. J. Magn. Reson. Imaging 2007, 25:48-54.
67. Zatorre R.J., Fields R.D., Johansen-Berg H. Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat. Neurosci. 2012, 15:528-536.
68. Zhang J., Jones M., DeBoy C.A., Reich D.S., Farrell J.A., Hoffman P.N., Griffin J.W., Sheikh K.A., Miller M.I., Mori S., Calabresi P.A. Diffusion tensor magnetic resonance imaging of Wallerian degeneration in rat spinal cord after dorsal root axotomy. J. Neurosci. 2009, 29:3160-3171.