Neural Correlates of Mirror Visual Feedback-Induced Performance Improvements: A Resting-State fMRI Study.

Viola Rjosk, Jöran Lepsien, Elisabeth Kaminski, Maike Hoff, Bernhard Sehm, Christopher J Steele, Arno Villringer, Patrick Ragert
Author Information
  1. Viola Rjosk: Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences Leipzig, Germany.
  2. Jöran Lepsien: Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences Leipzig, Germany.
  3. Elisabeth Kaminski: Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences Leipzig, Germany.
  4. Maike Hoff: Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences Leipzig, Germany.
  5. Bernhard Sehm: Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences Leipzig, Germany.
  6. Christopher J Steele: Department of Neurology, Max Planck Institute for Human Cognitive and Brain SciencesLeipzig, Germany; Cerebral Imaging Centre, Department of Psychiatry, Douglas Mental Health Institute, McGill UniversityMontreal, QC, Canada.
  7. Arno Villringer: Department of Neurology, Max Planck Institute for Human Cognitive and Brain SciencesLeipzig, Germany; Mind and Brain Institute, Charité and Humboldt UniversityBerlin, Germany.
  8. Patrick Ragert: Department of Neurology, Max Planck Institute for Human Cognitive and Brain SciencesLeipzig, Germany; Institute for General Kinesiology and Exercise Science, University of LeipzigLeipzig, Germany.

Abstract

Mirror visual feedback (MVF) is a promising approach to enhance motor performance without training in healthy adults as well as in patients with focal brain lesions. There is preliminary evidence that a functional modulation within and between primary motor cortices as assessed with transcranial magnetic stimulation (TMS) might be one candidate mechanism mediating the observed behavioral effects. Recently, studies using task-based functional magnetic resonance imaging (fMRI) have indicated that MVF-induced functional changes might not be restricted to the primary motor cortex (M1) but also include higher order regions responsible for perceptual-motor coordination and visual attention. However, aside from these instantaneous task-induced brain changes, little is known about learning-related neuroplasticity induced by MVF. Thus, in the present study, we assessed MVF-induced functional network plasticity with resting-state fMRI (rs-fMRI). We performed rs-fMRI of 35 right-handed, healthy adults before and after performing a complex ball-rotation task. The primary outcome measure was the performance improvement of the untrained left hand (LH) before and after right hand (RH) training with MVF (mirror group [MG], = 17) or without MVF (control group [CG], = 18). Behaviorally, the MG showed superior performance improvements of the untrained LH. In resting-state functional connectivity (rs-FC), an interaction analysis between groups showed changes in left visual cortex (V1, V2) revealing an increase of centrality in the MG. Within group comparisons showed further functional alterations in bilateral primary sensorimotor cortex (SM1), left V4 and left anterior intraparietal sulcus (aIP) in the MG, only. Importantly, a correlation analysis revealed a linear positive relationship between MVF-induced improvements of the untrained LH and functional alterations in left SM1. Our results suggest that MVF-induced performance improvements are associated with functional learning-related brain plasticity and have identified additional target regions for non-invasive brain stimulation techniques, a finding of potential interest for neurorehabilitation.

Keywords

References

  1. Neuroimage. 2007 Oct 1;37(4):1091-6; discussion 1097-9 [PMID: 17368915]
  2. Neuroimage. 2015 May 15;112:278-87 [PMID: 25770990]
  3. Neuroscientist. 2014 Oct;20(5):522-33 [PMID: 24561514]
  4. J Physiol. 1994 Mar 1;475(2):217-27 [PMID: 8021829]
  5. Curr Biol. 2009 Jun 23;19(12):1023-7 [PMID: 19427210]
  6. J Neurosci. 2012 Jan 25;32(4):1293-300 [PMID: 22279214]
  7. Neurorehabil Neural Repair. 2015 May;29(4):349-61 [PMID: 25160567]
  8. PLoS Biol. 2006 Apr;4(4):e100 [PMID: 16602824]
  9. J Neurophysiol. 2015 Apr 1;113(7):2383-9 [PMID: 25632079]
  10. Brain Connect. 2012;2(5):265-74 [PMID: 23016836]
  11. J Neurosci. 2015 Jul 8;35(27):9786-98 [PMID: 26156982]
  12. Nat Rev Neurosci. 2007 Sep;8(9):700-11 [PMID: 17704812]
  13. PLoS One. 2015 Oct 30;10(10):e0141828 [PMID: 26517375]
  14. Behav Brain Sci. 2004 Feb;27(1):3-24; discussion 24-78 [PMID: 15481943]
  15. PLoS One. 2010 Apr 27;5(4):e10232 [PMID: 20436911]
  16. Neuroimage. 2015 May 15;112:267-77 [PMID: 25770991]
  17. J Neurosci. 2011 Nov 23;31(47):16907-15 [PMID: 22114261]
  18. Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13848-53 [PMID: 16945915]
  19. Exp Brain Res. 2013 May;227(1):79-83 [PMID: 23543104]
  20. Stroke Res Treat. 2013;2013:128641 [PMID: 23738231]
  21. Arch Phys Med Rehabil. 2008 Mar;89(3):393-8 [PMID: 18295613]
  22. Cochrane Database Syst Rev. 2012 Mar 14;(3):CD008449 [PMID: 22419334]
  23. Neural Regen Res. 2013 Mar 5;8(7):639-46 [PMID: 25206709]
  24. Neuroimage. 2011 Sep 1;58(1):226-33 [PMID: 21689765]
  25. Neuropsychologia. 1971 Mar;9(1):97-113 [PMID: 5146491]
  26. Neuron. 2011 Nov 3;72(3):443-54 [PMID: 22078504]
  27. Cogn Neuropsychol. 2016 Feb-Mar;33(1-2):48-66 [PMID: 27314449]
  28. Exp Brain Res. 2008 Mar;185(3):509-19 [PMID: 17989973]
  29. Curr Opin Neurobiol. 2005 Dec;15(6):626-31 [PMID: 16271458]
  30. Neurorehabil Neural Repair. 2012 Jun;26(5):484-96 [PMID: 22247501]
  31. Curr Biol. 2007 Nov 6;17(21):1896-902 [PMID: 17964167]
  32. Pain. 2009 Aug;144(3):314-9 [PMID: 19501965]
  33. Neurorehabil Neural Repair. 2009 Mar-Apr;23(3):209-17 [PMID: 19074686]
  34. Lancet. 1999 Jun 12;353(9169):2035-6 [PMID: 10376620]
  35. J Jpn Phys Ther Assoc. 2013;16(1):1-6 [PMID: 25792898]
  36. Front Hum Neurosci. 2016 Jan 20;9:702 [PMID: 26834605]
  37. J Neurophysiol. 2003 Jan;89(1):168-76 [PMID: 12522169]
  38. Neural Plast. 2016;2016:6087896 [PMID: 26881121]
  39. Neuroimage. 2011 Aug 15;57(4):1492-8 [PMID: 21672633]
  40. Clin Neurophysiol. 2009 Oct;120(10):1859-65 [PMID: 19766535]
  41. Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17558-63 [PMID: 19805061]
  42. Exp Brain Res. 1991;83(2):419-26 [PMID: 2022247]
  43. Arch Phys Med Rehabil. 2009 Apr;90(4):675-81 [PMID: 19345786]
  44. Neurorehabil Neural Repair. 2011 Mar-Apr;25(3):223-33 [PMID: 21051765]
  45. Neuropsychologia. 2015 May;71:46-51 [PMID: 25796410]
  46. Nat Neurosci. 2015 Dec;18(12):1853-60 [PMID: 26551545]
  47. Trends Cogn Sci. 2007 Jun;11(6):229-35 [PMID: 17475536]
  48. Cerebellum. 2004;3(4):204-11 [PMID: 15686098]
  49. Restor Neurol Neurosci. 2014;32(2):269-80 [PMID: 24240987]
  50. Trends Neurosci. 1992 Jan;15(1):20-5 [PMID: 1374953]
  51. J Appl Physiol (1985). 2006 Nov;101(5):1514-22 [PMID: 17043329]
  52. Front Syst Neurosci. 2012 May 16;6:37 [PMID: 22623914]
  53. Science. 2007 Oct 26;318(5850):594-8 [PMID: 17962551]
  54. Eur J Neurosci. 2015 May;41(11):1475-83 [PMID: 25912048]
  55. Curr Biol. 2006 Dec 5;16(23):R998-1000 [PMID: 17141608]
  56. J Neurosci. 2010 Sep 1;30(35):11670-7 [PMID: 20810887]
  57. Exp Brain Res. 2005 May;163(1):118-22 [PMID: 15754176]
  58. Cereb Cortex. 2009 Oct;19(10):2209-29 [PMID: 19221144]
  59. Hum Brain Mapp. 2011 Feb;32(2):218-28 [PMID: 20336657]
  60. Neuropsychologia. 2005;43(2):301-12 [PMID: 15707914]
  61. Magn Reson Med. 1995 Oct;34(4):537-41 [PMID: 8524021]

Word Cloud

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