Skill learning strengthens cortical representations of motor sequences

eLife

Volumn 2013, Issue 2, 2013, Pages

  Wiestler, Tobias ^a   Diedrichsen, Jörn ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ARTICLE; BEHAVIORAL SCIENCE; ELECTROENCEPHALOGRAPHY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN EXPERIMENT; LEARNING; MALE; NORMAL HUMAN; PREDICTION; SEQUENCE ANALYSIS; TEMPORAL ANALYSIS; TRAINING; BEHAVIOR; HUMAN; MOTOR CORTEX; MULTIVARIATE ANALYSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE;

BEHAVIOR; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; MOTOR CORTEX; MULTIVARIATE ANALYSIS; PSYCHOMOTOR PERFORMANCE;

EID: 84880113516     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00801     Document Type: Article

References (52)

1. Churchland MM, Cunningham JP, Kaufman MT, Foster JD, Nuyujukian P, Ryu SI, et al. 2012. Neural population dynamics during reaching. Nature 487:51-6. doi: 10.1038/nature11129.
2. Culham JC, Valyear KF. 2006. Human parietal cortex in action. Curr Opin Neurobiol 16:205-12. doi: 10.1016/j.conb.2006.03.005.
3. Dale AM, Fischl B, Sereno MI. 1999. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179-94. doi: 10.1006/nimg.1998.0395.
4. Dayan E, Cohen LG. 2011. Neuroplasticity subserving motor skill learning. Neuron 72:443-54. doi: 10.1016/j.neuron.2011.10.008.
5. Diedrichsen J, Shadmehr R. 2005. Detecting and adjusting for artifacts in fMRI time series data. Neuroimage 27:624-34. doi: 10.1016/j.neuroimage.2005.04.039.
6. Diedrichsen J, Ridgway GR, Friston KJ, Wiestler T. 2011. Comparing the similarity and spatial structure of neural representations: a pattern-component model. Neuroimage 55:1665-78. doi: 10.1016/j.neuroimage.2011.01.044.
7. Diedrichsen J, Wiestler T, Ejaz N. 2013. A multivariate method to determine the dimensionality of neural representation from population activity. Neuroimage 76:225-35. doi: 10.1016/j.neuroimage.2013.02.062.
8. Diedrichsen J, Wiestler T, Krakauer JW. 2012. Two distinct ipsilateral cortical representations for Individuated finger movements. Cereb Cortex 23:1362-77. doi: 10.1093/cercor/bhs120.
9. Duda RO, Hart PE, Stork DG. 2001. Pattern classification. Hoboken, NJ: Wiley.
10. Farooqui AA, Mitchell D, Thompson R, Duncan J. 2012. Hierarchical organization of cognition reflected in distributed frontoparietal activity. J Neurosci 32:17373-81. doi: 10.1523/JNEUROSCI.0598-12.2012.
11. Fischl B, Rajendran N, Busa E, Augustinack J, Hinds O, Yeo BT, et al. 2008. Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex 18:1973-80. doi: 10.1093/cercor/bhm225.
12. Floyer-Lea A, Matthews PM. 2005. Distinguishable brain activation networks for short-and long-term motor skill learning. J Neurophysiol 94:512-8. doi: 10.1152/jn.00717.2004.
13. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F, Rizzolatti G. 2005. Parietal lobe: from action organization to intention understanding. Science 308:662-7. doi: 10.1126/science.1106138.
14. Freeman J, Brouwer GJ, Heeger DJ, Merriam EP. 2011. Orientation decoding depends on maps, not columns. J Neurosci 31:4792-804. doi: 10.1523/JNEUROSCI.5160-10.2011.
15. Gallivan JP, Mclean DA, Flanagan JR, Culham JC. 2013. Where one hand meets the other: limb-specific and action-dependent movement plans decoded from preparatory signals in single human frontoparietal brain areas. J Neurosci 33:1991-2008. doi: 10.1523/JNEUROSCI.0541-12.2013.
16. Gerloff C, Corwell B, Chen R, Hallett M, Cohen LG. 1997. Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. Brain 120(Pt 9):1587-602. doi: 10.1093/brain/120.9.1587.
17. Grafton ST, Hazeltine E, Ivry R. 1995. Functional mapping of sequence learning in normal humans. J Cogn Neurosci 7:497-510. doi: 10.1162/jocn.1995.7.4.497.
18. Hardwick RM, Rottschy C, Miall RC, Eickhoff SB. 2013. A quantitative meta-analysis and review of motor learning in the human brain. Neuroimage 67:283-97. doi: 10.1016/j.neuroimage.2012.11.020.
19. Hartwigsen G, Saur D, Price CJ, Baumgaertner A, Ulmer S, Siebner HR. 2013. Increased facilitatory connectivity from the pre-SMA to the left dorsal premotor cortex during pseudoword repetition. J Cogn Neurosci 25:580-94. doi: 10.1162/jocn_a_00342.
20. Hazeltine E, Grafton ST, Ivry R. 1997. Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study. Brain 120(Pt 1):123-40. doi: 10.1093/brain/120.1.123.
21. Heim S, Amunts K, Hensel T, Grande M, Huber W, Binkofski F, et al. 2012. The role of human parietal area 7A as a link between sequencing in hand actions and in overt speech production. Front Psychol 3:534. doi: 10.3389/fpsyg.2012.00534.
22. Huang Y, Zhen Z, Song Y, Zhu Q, Wang S, Liu J. 2013. Motor training increases the stability of activation patterns in the primary motor cortex. PLOS ONE 8:e53555. doi: 10.1371/journal.pone.0053555.
23. Hutton C, Bork A, Josephs O, Deichmann R, Ashburner J, Turner R. 2002. Image distortion correction in fMRI: a quantitative evaluation. Neuroimage 16:217-40. doi: 10.1006/nimg.2001.1054.
24. Jenkins IH, Brooks DJ, Nixon PD, Frackowiak RS, Passingham RE. 1994. Motor sequence learning: a study with positron emission tomography. J Neurosci 14:3775-90.
25. Kamitani Y, Tong F. 2005. Decoding the visual and subjective contents of the human brain. Nat Neurosci 8:679-85. doi: 10.1038/nn1444.
26. Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG. 1995. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377:155-8. doi: 10.1038/377155a0.
27. Kay KN, David SV, Prenger RJ, Hansen KA, Gallant JL. 2008. Modeling low-frequency fluctuation and hemodynamic response timecourse in event-related fMRI. Hum Brain Mapp 29:142-56. doi: 10.1002/hbm.20379.
28. Keele SW, Jennings P, Jones S, Caulton D, Cohen A. 1995. On the modularity of sequence representation. J Motor Behav 27:17-30. doi: 10.1080/00222895.1995.9941696.
29. Kennerley SW, Sakai K, Rushworth MF. 2004. Organization of action sequences and the role of the pre-SMA. J Neurophysiol 91:978-93. doi: 10.1152/jn.00651.2003.
30. Kiebel SJ, Von Kriegstein K, Daunizeau J, Friston KJ. 2009. Recognizing sequences of sequences. PLOS Comput Biol 5:e1000464. doi: 10.1371/journal.pcbi.1000464.
31. Kornysheva K, Sierk A, Diedrichsen J. 2013. Interaction of temporal and ordinal representations in movement sequences. J Neurophysiol 109:1416-24. doi: 10.1152/jn.00509.2012.
32. Lehericy S, Benali H, Van De Moortele PF, Pelegrini-Issac M, Waechter T, Ugurbil K, et al. 2005. Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proc Natl Acad Sci USA 102:12566-71. doi: 10.1073/pnas.0502762102.
33. Ma L, Wang B, Narayana S, Hazeltine E, Chen X, Robin DA, et al. 2010. Changes in regional activity are accompanied with changes in inter-regional connectivity during 4 weeks motor learning. Brain Res 1318:64-76. doi: 10.1016/j.brainres.2009.12.073.
34. Matsuzaka Y, Picard N, Strick PL. 2007. Skill representation in the primary motor cortex after long-term practice. J Neurophysiol 97:1819-32. doi: 10.1152/jn.00784.2006.
35. Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM. 1996. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16:785-807.
36. Oosterhof NN, Wiestler T, Downing PE, Diedrichsen J. 2011. A comparison of volume-based and surface-based multi-voxel pattern analysis. Neuroimage 56:593-600. doi: 10.1016/j.neuroimage.2010.04.270.
37. Penhune VB, Doyon J. 2002. Dynamic cortical and subcortical networks in learning and delayed recall of timed motor sequences. J Neuroscience 22:1397-406.
38. Penhune VB, Doyon J. 2005. Cerebellum and M1 interaction during early learning of timed motor sequences. Neuroimage 26:801-12. doi: 10.1016/j.neuroimage.2005.02.041.
39. Penhune VB, Steele CJ. 2012. Parallel contributions of cerebellar, striatal and M1 mechanisms to motor sequence learning. Behav Brain Res 226:579-91. doi: 10.1016/j.bbr.2011.09.044.
40. Poldrack RA. 2000. Imaging brain plasticity: conceptual and methodological issues-a theoretical review. Neuroimage 12:1-13. doi: 10.1006/nimg.2000.0596.
41. Poldrack RA, Sabb FW, Foerde K, Tom SM, Asarnow RF, Bookheimer SY, et al. 2005. The neural correlates of motor skill automaticity. J Neurosci 25:5356-64. doi: 10.1523/JNEUROSCI.3880-04.2005.
42. Shima K, Tanji J. 1998. Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J Neurophysiol 80:3247-60.
43. Steele CJ, Penhune VB. 2010. Specific increases within global decreases: a functional magnetic resonance imaging investigation of five days of motor sequence learning. J Neurosci 30:8332-41. doi: 10.1523/JNEUROSCI.5569-09.2010.
44. Swisher JD, Gatenby JC, Gore JC, Wolfe BA, Moon CH, Kim SG, et al. 2010. Multiscale pattern analysis of orientation-selective activity in the primary visual cortex. J Neurosci 30:325-30. doi: 10.1523/JNEUROSCI.4811-09.2010.
45. Tanji J, Shima K. 1994. Role for supplementary motor area cells in planning several movements ahead. Nature 371:413-6. doi: 10.1038/371413a0.
46. Toni I, Krams M, Turner R, Passingham RE. 1998. The time course of changes during motor sequence learning: a whole-brain fMRI study. Neuroimage 8:50-61. doi: 10.1006/nimg.1998.0349.
47. Ungerleider LG, Doyon J, Karni A. 2002. Imaging brain plasticity during motor skill learning. Neurobiol Learn Mem 78:553-64. doi: 10.1006/nlme.2002.4091.
48. Verstynen T, Diedrichsen J, Albert N, Aparicio P, Ivry RB. 2005. Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. J Neurophysiol 93:1209-22. doi: 10.1152/jn.00720.2004.
49. Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC. 1996. A unified statistical approach for determining significant voxels in images of cerebral activation. Human Brain Mapping 12:900-18.
50. Wu T, Kansaku K, Hallett M. 2004. How self-initiated memorized movements become automatic: a functional MRI study. J Neurophysiol 91:1690-8. doi: 10.1152/jn.01052.2003.
51. Xiong J, Ma L, Wang B, Narayana S, Duff EP, Egan GF, et al. 2009. Long-term motor training induced changes in regional cerebral blood flow in both task and resting states. Neuroimage 45:75-82. doi: 10.1016/j.neuroimage.2008.11.016.
52. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, et al. 1997. Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120(Pt 1):141-57. doi: 10.1093/brain/120.1.141.