Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2011, Article ID 871296, 9 pages
http://dx.doi.org/10.1155/2011/871296
Review Article

Cortical Plasticity during Motor Learning and Recovery after Ischemic Stroke

1Clinical Neurorehabilitation, Department of Neurology, University of Zurich, 8091 Zurich, Switzerland
2Rehabilitation Institute and Technology Center (RITZ), 8008 Zurich, Switzerland
3Division of Brain Injury Outcomes, Department of Neurology, Johns Hopkins University, Baltimore, MD 21231, USA

Received 21 April 2011; Revised 18 July 2011; Accepted 22 August 2011

Academic Editor: Anja Gundlfinger

Copyright © 2011 Jonas A. Hosp and Andreas R. Luft. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. Rosamond, K. Flegal, G. Friday et al., “Heart disease and stroke statistics—2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee,” Circulation, vol. 115, no. 5, pp. e69–e171, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. B. Kolb and I. Q. Whishaw, “Brain plasticity and behavior,” Annual Review of Psychology, vol. 49, pp. 43–64, 1998. View at Google Scholar · View at Scopus
  3. C. Xerri, J. O. Coq, M. M. Merzenich, and W. M. Jenkins, “Experience-induced plasticity of cutanaeous maps in the primary somatosensory cortex of adult monkeys and rats,” Journal of Physiology Paris, vol. 90, no. 3-4, pp. 277–287, 1996. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Asanuma and C. Pavlides, “Neurobiological basis of motor learning in mammals,” NeuroReport, vol. 8, no. 4, pp. R1–R6, 1997. View at Google Scholar · View at Scopus
  5. A. R. Luft, M. M. Buitrago, A. Kaelin-Lang, J. Dichgans, and J. B. Schulz, “Protein synthesis inhibition blocks consolidation of an acrobatic motor skill,” Learning and Memory, vol. 11, no. 4, pp. 379–382, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. A. R. Luft, M. M. Buitrago, T. Ringer, J. Dichgans, and J. B. Schulz, “Motor skill learning depends on protein synthesis in motor cortex after training,” Journal of Neuroscience, vol. 24, no. 29, pp. 6515–6520, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. M. H. Monfils, E. J. Plautz, and J. A. Kleim, “In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience,” Neuroscientist, vol. 11, no. 5, pp. 471–483, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. R. J. Nudo, “Neurophysiology of motor skill learning,” in Learning and Memory: A Comprehensive Reference, Chapter 3.21, pp. 403–421, Academic Press, 2008. View at Google Scholar
  9. A. Keller, “Intrinsic synaptic organization of the motor cortex,” Cerebral Cortex, vol. 3, no. 5, pp. 430–441, 1993. View at Google Scholar · View at Scopus
  10. M. H. Schieber, “Constraints on somatotopic organization in the primary motor cortex,” Journal of Neurophysiology, vol. 86, no. 5, pp. 2125–2143, 2001. View at Google Scholar · View at Scopus
  11. R. J. Nudo, E. J. Plautz, and S. B. Frost, “Role of adaptive plasticity in recovery of function after damage to motor cortex,” Muscle and Nerve, vol. 24, no. 8, pp. 1000–1019, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. J. N. Sanes and M. H. Schieber, “Orderly somatotopy in primary motor cortex: does it exist?” NeuroImage, vol. 13, no. 6, pp. 968–974, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Molina-Luna, M. M. Buitrago, B. Hertler et al., “Cortical stimulation mapping using epidurally implanted thin-film microelectrode arrays,” Journal of Neuroscience Methods, vol. 161, no. 1, pp. 118–125, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Gioanni and M. Lamarche, “A reappraisal of rat motor cortex organization by intracortical microstimulation,” Brain Research, vol. 344, no. 1, pp. 49–61, 1985. View at Publisher · View at Google Scholar · View at Scopus
  15. E. J. Neafsey, E. L. Bold, G. Haas et al., “The organization of the rat motor cortex: a microstimulation mapping study,” Brain Research Reviews, vol. 11, no. 1, pp. 77–96, 1986. View at Publisher · View at Google Scholar
  16. J. A. Kleim, S. Barbay, and R. J. Nudo, “Functional reorganization of the rat motor cortex following motor skill learning,” Journal of Neurophysiology, vol. 80, no. 6, pp. 3321–3325, 1998. View at Google Scholar · View at Scopus
  17. R. J. Nudo, G. W. Milliken, W. M. Jenkins, and M. M. Merzenich, “Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys,” Journal of Neuroscience, vol. 16, no. 2, pp. 785–807, 1996. View at Google Scholar · View at Scopus
  18. A. Pascual-Leone, N. Dang, L. G. Cohen, J. P. Brasil-Neto, A. Cammarota, and M. Hallett, “Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills,” Journal of Neurophysiology, vol. 74, no. 3, pp. 1037–1045, 1995. View at Google Scholar · View at Scopus
  19. J. A. Kleim, T. M. Hogg, P. M. VandenBerg, N. R. Cooper, R. Bruneau, and M. Remple, “Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning,” Journal of Neuroscience, vol. 24, no. 3, pp. 628–633, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. M. S. Remple, R. M. Bruneau, P. M. VandenBerg, C. Goertzen, and J. A. Kleim, “Sensitivity of cortical movement representations to motor experience: evidence that skill learning but not strength training induces cortical reorganization,” Behavioural Brain Research, vol. 123, no. 2, pp. 133–141, 2001. View at Publisher · View at Google Scholar
  21. K. Molina-Luna, B. Hertler, M. M. Buitrago, and A. R. Luft, “Motor learning transiently changes cortical somatotopy,” NeuroImage, vol. 40, no. 4, pp. 1748–1754, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. E. J. Plautz, G. W. Milliken, and R. J. Nudo, “Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning,” Neurobiology of Learning and Memory, vol. 74, no. 1, pp. 27–55, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. J. M. Conner, A. Culberson, C. Packowski, A. A. Chiba, and M. H. Tuszynski, “Lesions of the basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning,” Neuron, vol. 38, no. 5, pp. 819–829, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Hogg, D Vozar, PM VandenBerg, and JA Kleim, “Expansion of distal forelimb representation within rat motorcortex is dependent upon performance and not acquisition of skilled forelimb movements,” Society for Neuroscience Abstracts, vol. 27, 2001. View at Google Scholar
  25. A. Karni, G. Meyer, P. Jezzard, M. M. Adams, R. Turner, and L. G. Ungerleider, “Functional MRI evidence for adult motor cortex plasticity during motor skill learning,” Nature, vol. 377, no. 6545, pp. 155–158, 1995. View at Google Scholar · View at Scopus
  26. W. T. Greenough, J. R. Larson, and G. S. Withers, “Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex,” Behavioral and Neural Biology, vol. 44, no. 2, pp. 301–314, 1985. View at Google Scholar · View at Scopus
  27. G. S. Withers and W. T. Greenough, “Reach training selectively alters dendritic branching in subpopulations of layer II-III pyramids in rat motor-somatosensory forelimb cortex,” Neuropsychologia, vol. 27, no. 1, pp. 61–69, 1989. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Xu, X. Yu, A. J. Perlik et al., “Rapid formation and selective stabilization of synapses for enduring motor memories,” Nature, vol. 462, no. 7275, pp. 915–919, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. L. Wang, J. M. Conner, J. Rickert, and M. H. Tuszynski, “Structural plasticity within highly specific neuronal populations identifies a unique parcellation of motor learning in the adult brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 6, pp. 2545–2550, 2011. View at Publisher · View at Google Scholar
  30. G. Hess and J. P. Donoghue, “Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps,” Journal of Neurophysiology, vol. 71, no. 6, pp. 2543–2547, 1994. View at Google Scholar · View at Scopus
  31. R. J. Racine, C. A. Chapman, C. Trepel, G. C. Teskey, and N. W. Milgram, “Post-activation potentiation in the neocortex. IV. Multiple sessions required for induction of long-term potentiation in the chronic preparation,” Brain Research, vol. 702, no. 1-2, pp. 87–93, 1995. View at Publisher · View at Google Scholar · View at Scopus
  32. M. S. Rioult-Pedotti, D. Friedman, G. Hess, and J. P. Donoghue, “Strengthening of horizontal cortical connections following skill learning,” Nature Neuroscience, vol. 1, no. 3, pp. 230–234, 1998. View at Google Scholar · View at Scopus
  33. M. S. Rioult-Pedotti, D. Friedman, and J. P. Donoghue, “Learning-induced LTP in neocortex,” Science, vol. 290, no. 5491, pp. 533–536, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. M. S. Rioult-Pedotti, J. P. Donoghue, and A. Dunaevsky, “Plasticity of the synaptic modification range,” Journal of Neurophysiology, vol. 98, no. 6, pp. 3688–3695, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. M. H. Monfils and G. C. Teskey, “Skilled-learning-induced potentiation in rat sensorimotor cortex: a transient form of behavioural long-term potentiation,” Neuroscience, vol. 125, no. 2, pp. 329–336, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. M. H. Monfils, P. M. VandenBerg, J. A. Kleim, and G. C. Teskey, “Long-term potentiation induces expanded movement representations and dendritic hypertrophy in layer V of rat sensorimotor neocortex,” Cerebral Cortex, vol. 14, no. 5, pp. 586–593, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. M. H. Monfils and G. C. Teskey, “Induction of long-term depression is associated with decreased dendritic length and spine density in layers III and V of sensorimotor neocortex,” Synapse, vol. 53, no. 2, pp. 114–121, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. R. J. Nudo and G. W. Milliken, “Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys,” Journal of Neurophysiology, vol. 75, no. 5, pp. 2144–2149, 1996. View at Google Scholar · View at Scopus
  39. R. J. Nudo, B. M. Wise, F. SiFuentes, and G. W. Milliken, “Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct,” Science, vol. 272, no. 5269, pp. 1791–1794, 1996. View at Google Scholar · View at Scopus
  40. S. L. Wolf, C. J. Winstein, J. P. Miller et al., “Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial,” Journal of the American Medical Association, vol. 296, no. 17, pp. 2095–2104, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Barbay, E. J. Plautz, K. M. Friel et al., “Behavioral and neurophysiological effects of delayed training following a small ischemic infarct in primary motor cortex of squirrel monkeys,” Experimental Brain Research, vol. 169, no. 1, pp. 106–116, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Biernaskie and D. Corbett, “Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury,” Journal of Neuroscience, vol. 21, no. 14, pp. 5272–5280, 2001. View at Google Scholar · View at Scopus
  43. J. Biernaskie, G. Chernenko, and D. Corbett, “Efficacy of rehabilitative experience declines with time after focal ischemic brain injury,” Journal of Neuroscience, vol. 24, no. 5, pp. 1245–1254, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. R. Traversa, P. Cicinelli, A. Bassi, P. M. Rossini, and G. Bernardi, “Mapping of motor cortical reorganization after stroke: a brain simulation study with focal magnetic pulses,” Stroke, vol. 28, no. 1, pp. 110–117, 1997. View at Google Scholar · View at Scopus
  45. S. T. Carmichael, “Cellular and molecular mechanisms of neural repair after stroke: making waves,” Annals of Neurology, vol. 59, no. 5, pp. 735–742, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. S. C. Cramer, R. Shah, J. Juranek, K. R. Crafton, and V. Le, “Activity in the peri-infarct rim in relation to recovery from stroke,” Stroke, vol. 37, no. 1, pp. 111–115, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. C. E. Brown, J. D. Boyd, and T. H. Murphy, “Longitudinal in vivo imaging reveals balanced and branch-specific remodeling of mature cortical pyramidal dendritic arbors after stroke,” Journal of Cerebral Blood Flow and Metabolism, vol. 30, no. 4, pp. 783–791, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Mostany and C. Portera-Cailliau, “Absence of large-scale dendritic plasticity of layer 5 pyramidal neurons in peri-infarct cortex,” Journal of Neuroscience, vol. 31, no. 5, pp. 1734–1738, 2011. View at Publisher · View at Google Scholar
  49. C. E. Brown, C. Wong, and T. H. Murphy, “Rapid morphologic plasticity of peri-infarct dendritic spines after focal ischemic stroke,” Stroke, vol. 39, no. 4, pp. 1286–1291, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. R. J. Andrews, “Transhemispheric diaschisis. A review and comment,” Stroke, vol. 22, no. 7, pp. 943–949, 1991. View at Google Scholar · View at Scopus
  51. S. T. Carmichael, L. Wei, C. M. Rovainen, and T. A. Woolsey, “New patterns of intracortical projections after focal cortical stroke,” Neurobiology of Disease, vol. 8, no. 5, pp. 910–922, 2001. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Silver and J. H. Miller, “Regeneration beyond the glial scar,” Nature Reviews Neuroscience, vol. 5, no. 2, pp. 146–156, 2004. View at Google Scholar · View at Scopus
  53. D. Katsman, J. Zheng, K. Spinelli, and S. T. Carmichael, “Tissue microenvironments within functional cortical subdivisions adjacent to focal stroke,” Journal of Cerebral Blood Flow and Metabolism, vol. 23, no. 9, pp. 997–1009, 2003. View at Google Scholar · View at Scopus
  54. S. T. Carmichael, I. Archibeque, L. Luke, T. Nolan, J. Momiy, and S. Li, “Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex,” Experimental Neurology, vol. 193, no. 2, pp. 291–311, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. S. T. Carmichael, “Plasticity of cortical projections after stroke,” Neuroscientist, vol. 9, no. 1, pp. 64–75, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Li and S. T. Carmichael, “Growth-associated gene and protein expression in the region of axonal sprouting in the aged brain after stroke,” Neurobiology of Disease, vol. 23, no. 2, pp. 362–373, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. G. Hagemann, C. Redecker, T. Neumann-Haefelin, H.-J. Freund, and O. W. Witte, “Increased long-term potentiation in the surround of experimentally induced focal cortical infarction,” Annals of Neurology, vol. 44, no. 2, pp. 255–258, 1998. View at Publisher · View at Google Scholar
  58. M. W. Salter and L. V. Kalia, “SRC kinases: a hub for NMDA receptor regulation,” Nature Reviews Neuroscience, vol. 5, no. 4, pp. 317–328, 2004. View at Google Scholar · View at Scopus
  59. K. Schiene, C. Bruehl, K. Zilles et al., “Neuronal hyperexcitability and reduction of GABA(A)-receptor expression in the surround of cerebral photothrombosis,” Journal of Cerebral Blood Flow and Metabolism, vol. 16, no. 5, pp. 906–914, 1996. View at Google Scholar · View at Scopus
  60. S. B. Frost, S. Barbay, K. M. Friel, E. J. Plautz, and R. J. Nudo, “Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery,” Journal of Neurophysiology, vol. 89, no. 6, pp. 3205–3214, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Dancause, S. Barbay, S. B. Frost et al., “Effects of small ischemic lesions in the primary motor cortex on neurophysiological organization in ventral premotor cortex,” Journal of Neurophysiology, vol. 96, no. 6, pp. 3506–3511, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. Y. Liu and E. M. Rouiller, “Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys,” Experimental Brain Research, vol. 128, no. 1-2, pp. 149–159, 1999. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Weiller, F. Chollet, K. J. Friston, R. J. S. Wise, and R. S. J. Frackowiak, “Functional reorganization of the brain in recovery from striatocapsular infarction in man,” Annals of Neurology, vol. 31, no. 5, pp. 463–472, 1992. View at Google Scholar · View at Scopus
  64. A. R. Luft, S. McCombe-Waller, J. Whitall et al., “Repetitive bilateral arm training and motor cortex activation in chronic stroke: a randomized controlled trial,” Journal of the American Medical Association, vol. 292, no. 15, pp. 1853–1861, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. N. Dancause, S. Barbay, S. B. Frost et al., “Extensive cortical rewiring after brain injury,” Journal of Neuroscience, vol. 25, no. 44, pp. 10167–10179, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. I. Eisner-Janowicz, S. Barbay, E. Hoover et al., “Early and late changes in the distal forelimb representation of the supplementary motor area after injury to frontal motor areas in the squirrel monkey,” Journal of Neurophysiology, vol. 100, no. 3, pp. 1498–1512, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. J. R. Carey, T. J. Kimberley, S. M. Lewis et al., “Analysis of fMRI and finger tracking training in subjects with chronic stroke,” Brain, vol. 125, no. 4, pp. 773–788, 2002. View at Google Scholar · View at Scopus
  68. T. A. Jones and T. Schallert, “Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage,” Brain Research, vol. 581, no. 1, pp. 156–160, 1992. View at Publisher · View at Google Scholar · View at Scopus
  69. T. A. Jones, J. A. Kleim, and W. T. Greenough, “Synaptogenesis and dendritic growth in the cortex opposite unilateral sensorimotor cortex damage in adult rats: a quantitative electron microscopic examination,” Brain Research, vol. 733, no. 1, pp. 142–148, 1996. View at Publisher · View at Google Scholar · View at Scopus
  70. T. A. Jones and T. Schallert, “Use-dependent growth of pyramidal neurons after neocortical damage,” Journal of Neuroscience, vol. 14, no. 4, pp. 2140–2152, 1994. View at Google Scholar · View at Scopus
  71. H. Nhan, K. Barquist, K. Bell, P. Esselman, I. R. Odderson, and S. C. Cramer, “Brain function early after stroke in relation to subsequent recovery,” Journal of Cerebral Blood Flow and Metabolism, vol. 24, no. 7, pp. 756–763, 2004. View at Google Scholar · View at Scopus
  72. N. S. Ward, M. M. Brown, A. J. Thompson, and R. S. J. Frackowiak, “The influence of time after stroke on brain activations during a motor task,” Annals of Neurology, vol. 55, no. 6, pp. 829–834, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. L. M. Carey, D. F. Abbott, G. F. Egan et al., “Evolution of brain activation with good and poor motor recovery after stroke,” Neurorehabilitation and Neural Repair, vol. 20, no. 1, pp. 24–41, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Liepert, W. H. R. Miltner, H. Bauder et al., “Motor cortex plasticity during constraint,induced movement therapy in stroke patients,” Neuroscience Letters, vol. 250, no. 1, pp. 5–8, 1998. View at Publisher · View at Google Scholar · View at Scopus
  75. J. H. Carr and R. B. Shepherd, A Motor Relearning Programme for Stroke, Butterworth Heinemann, Oxford, UK, 1987.
  76. M. Schubring-Giese, K. Molina-Luna, B. Hertler, M. M. Buitrago, D. F. Hanley, and A. R. Luft, “Speed of motor re-learning after experimental stroke depends on prior skill,” Experimental Brain Research, vol. 181, no. 2, pp. 359–365, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. R. V. Krishnan, “Relearning toward motor recovery in stroke, spinal cord injury, and cerebral palsy: a cognitive neural systems perspective,” International Journal of Neuroscience, vol. 116, no. 2, pp. 127–140, 2006. View at Publisher · View at Google Scholar · View at Scopus