Recovery after brain injury: Mechanisms and principles

Frontiers in Human Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Nudo, Randolph J ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Axonal sprouting; Motor cortex; Motor learning; Recovery; Stroke; Traumatic brain injury

Indexed keywords

ADAPTIVE BEHAVIOR; ARTICLE; GABAERGIC SYSTEM; HUMAN; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALADAPTIVE BEHAVIOR; MOTOR ACTIVITY; MOTOR CORTEX; MOTOR PERFORMANCE; MUSCLE CONTRACTION; NEGATIVE FEEDBACK; NERVE CELL PLASTICITY; NERVE SPROUTING; NONHUMAN; SENSORY STIMULATION; SOMATOSENSORY CORTEX; TRANSCRANIAL MAGNETIC STIMULATION; TRAUMATIC BRAIN INJURY;

EID: 84891637337     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2013.00887     Document Type: Article

References (100)

1. Allred, R. P., and Jones, T. A. (2008). Maladaptive effects of learning with the less- affected forelimb after focal cortical infarcts in rats. Exp. Neurol. 210, 172-181. doi: 10.1016/j.expneurol.2007.10.010
2. Allred, R. P., Maldonado, M. A., Hsu, J.e., and Jones, T. A. (2005). Training the "less-affected" forelimb after unilateral cortical infarcts interferes with functional recovery of the impaired forelimb in rats. Restor. Neurol. Neurosci. 23, 297-302.
3. Aroniadou, V. A., and Keller, A. (1993). The patterns and synaptic properties of horizontal intracortical connections in the rat motor cortex. J. Neurophysiol. 70, 1553-1569.
4. Biernaskie, J., Szymanska, A., Windle, V., and Corbett, D. (2005). Bi-hemispheric contribution to functional motor recovery of the affected forelimb following focal ischemic brain injury in rats. Eur. J. Neurosci. 21, 989-999. doi: 10.1111/j.1460-9568.2005.03899.x
5. Birkenmeier, R. L., Prager, E. M., and Lang, C. E. (2010). Translating animal doses of task-specific training to people with chronic stroke in 1-hour therapy sessions: a proof-of-concept study. Neurorehabil. Neural Repair 24, 620-635. doi: 10.1177/1545968310361957
6. Brown, C. E., Boyd, J. D., and Murphy, T. H. (2010). Longitudinal in vivo imaging reveals balanced and branch-specific remodeling of mature cortical pyramidal dendritic arbors after stroke. J. Cereb. Blood Flow Metab. 30, 783-791. doi: 10.1038/jcbfm.2009.241
7. Brown, C. E., Li, P., Boyd, J. D., Delaney, K. R., and Murphy, T. H. (2007). Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J. Neurosci. 27, 4101-4109. doi: 10.1523/JNEUROSCI.4295-06.2007
8. Brown, C. E., and Murphy, T. H. (2008). Livin' on the edge: imaging dendritic spine turnover in the peri-infarct zone during ischemic stroke and recovery. Neuroscientist 14, 139-146. doi: 10.1177/1073858407309854
9. Bury, S. D., and Jones, T. A. (2004). Facilitation of motor skill learning by callosal denervation or forced forelimb use in adult rats. Behav. Brain Res. 150, 43-53. doi: 10.1016/S0166-4328(03)00253-5
10. Butefisch, C. M., Kleiser, R., and Seitz, R. J. (2006). Post-lesional cerebral reorganisation: evidence from functional neuroimaging and transcranial magnetic stimulation. J. Physiol. Paris 99, 437-454. doi: 10.1016/j.jphysparis.2006.03.001
11. Capaday, C., Ethier, C., Van Vreeswijk, C., and Darling, W. G. (2013). On the functional organization and operational principles of the motor cortex. Front. Neural Circuits 7:66. doi: 10.3389/fncir.2013.00066
12. Carey, J. R., Kimberley, T. J., Lewis, S. M., Auerbach, E. J., Dorsey, L., Rundquist, P., et al. (2002). Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain 125(Pt 4), 773-788. doi: 10.1093/brain/awf091
13. Carmichael, S. T. (2006). Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann. Neurol. 59, 735-742. doi: 10.1002/ana.20845
14. Carmichael, S. T., and Chesselet, M. F. (2002). Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. J. Neurosci. 22, 6062-6070.
15. Cheung, V. C., Deboer, C., Hanson, E., Tunesi, M., D'Onofrio, M., Arisi, I., et al. (2013). Gene expression changes in the motor cortex mediating motor skill learning. PLoS ONE 8:e61496. doi: 10.1371/journal.pone.0061496
16. Chollet, F., DiPiero, V., Wise, R. J., Brooks, D. J., Dolan, R. J., and Frackowiak, R. S. (1991). The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann. Neurol. 29, 63-71. doi: 10.1002/ana.410290112
17. Cirstea, M. C., and Levin, M. F. (2000). Compensatory strategies for reaching in stroke. Brain 123(Pt 5), 940-953. doi: 10.1093/brain/123.5.940
18. Clarkson, A. N., Lopez-Valdes, H. E., Overman, J. J., Charles, A. C., Brennan, K. C., and Thomas Carmichael, S. (2013). Multimodal examination of structural and functional remapping in the mouse photothrombotic stroke model. J. Cereb. BloodFlowMetab. 33, 716-723. doi: 10.1038/jcbfm.2013.7
19. Cooke, E. V., Mares, K., Clark, A., Tallis, R. C., and Pomeroy, V. M. (2010). The effects of increased dose of exercise-based therapies to enhance motor recovery after stroke: a systematic review and meta-analysis. BMC Med. 8:60. doi: 10.1186/1741-7015-8-60
20. Cramer, S. C. (2000). Stroke recovery: how the computer reprograms itself. Neuronal plasticity: the key to stroke recovery. Kananskis, Alberta, Canada, 19-22 March 2000. Mol. Med. Today 6, 301-303. doi: 10.1016/S1357- 4310(00)01744-5
21. Cramer, S. C., Nelles, G., Benson, R. R., Kaplan, J. D., Parker, R. A., Kwong, K. K., et al. (1997). A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28, 2518-2527. doi: 10.1161/01.STR.28.12.2518
22. Dancause, N., Barbay, S., Frost, S. B., Plautz, E. J., Chen, D., Zoubina, E. V., et al. (2005). Extensive cortical rewiring after brain injury. J. Neurosci. 25, 10167-10179. doi: 10.1523/JNEUROSCI.3256-05.2005
23. Enright, L. E., Zhang, S., and Murphy, T. H. (2007). Fine mapping of the spatial relationship between acute ischemia and dendritic structure indicates selective vulnerability of layer V neuron dendritic tufts within single neurons in vivo. J. Cereb. Blood Flow Metab. 27, 1185-1200. doi: 10.1038/sj.jcbfm.9600428
24. Fridman, E. A., Hanakawa, T., Chung, M., Hummel, F., Leiguarda, R. C., and Cohen, L. G. (2004). Reorganization of the human ipsilesional premotor cortex after stroke. Brain 127(Pt 4), 747-758. doi: 10.1093/brain/awh082
25. Friel, K. M., Barbay, S., Frost, S. B., Plautz, E. J., Hutchinson, D. M., Stowe, A. M., et al. (2005). Dissociation of sensorimotor deficits after rostral versus caudal lesions in the primary motor cortex hand representation. J. Neurophysiol. 94, 1312-1324. doi: 10.1152/jn.01251.2004
26. Frost, S. B., Barbay, S., Friel, K. M., Plautz, E. J., and Nudo, R. J. (2003). Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J. Neurophysiol. 89, 3205-3214. doi: 10.1152/jn.01143.2002
27. Glees, P., and Cole, J. (1949). The reappearance of coordinated movements of the hand after lesions in the hand area of the motor cortex of the rhesus monkey. J. Physiol. 108, 33.
28. Griffin, D. M., Hudson, H. M., Belhaj-Saif, A., and Cheney, P. D. (2009). Stability of output effects from motor cortex to forelimb muscles in primates. J. Neurosci. 29, 1915-1927. doi: 10.1523/JNEUR0SCI.4831-08.2009
29. Hammond, G. (2002). Correlates of human handedness in primary motor cortex: a review and hypothesis. Neurosci. Biobehav. Rev. 26, 285-292. doi: 10.1016/S0149-7634(02)00003-9
30. Harms, K. J., Rioult-Pedotti, M. S., Carter, D. R., and Dunaevsky, A. (2008). Transient spine expansion and learning-induced plasticity in layer 1 primary motor cortex. J. Neurosci. 28, 5686-5690. doi: 10.1523/JNEUROSCI.0584-08.2008
31. Harrison, T. C., Silasi, G., Boyd, J. D., and Murphy, T. H. (2013). Displacement of sensorymaps and disorganization of motor cortex after targeted stroke in mice. Stroke 44,2300-2306. doi: 10.1161/STR0KEAHA.113.001272
32. Hess, G., Aizenman, C. D., and Donoghue, J. P. (1996). Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. J. Neurophysiol. 75, 1765-1778.
33. Hosp, J. A., and Luft, A. R. (2013). Dopaminergic meso-cortical projections to M1: role in motor learning and motor cortex plasticity. Front. Neurol. 4:145. doi: 10.3389/fneur.2013.00145
34. Hsieh, Y. W., Wu, C. Y., Liao, W. W., Lin, K. C., Wu, K. Y., and Lee, C. Y. (2011). Effects of treatment intensity in upper limb robot-assisted therapy for chronic stroke: a pilot randomized controlled trial. Neurorehabil. Neural Repair 25, 503-511. doi: 10.1177/1545968310394871
35. Humm, J. L., Kozlowski, D. A., Bland, S. T., James, D. C., and Schallert, T. (1999). Use-dependent exaggeration ofbrain injury: is glutamate involved? Exp. Neurol. 157, 349-358. doi: 10.1006/exnr.1999.7061
36. Huntley, G. W., and Jones, E. G. (1991). Relationship of intrinsic connections to forelimb movement representations in monkey motor cortex: a correlative anatomic and physiological study. J. Neurophysiol. 66, 390-413.
37. Jackson, A., Mavoori, J., and Fetz, E. E. (2006). Long-term motor cortex plasticity induced by an electronic neural implant. Nature 444, 56-60. doi: 10.1038/nature05226
38. Jaillard, A., Martin, C. D., Garambois, K., Lebas, J. F., and Hommel, M. (2005). Vicarious function within the human primary motor cortex? A longitudinal fMRI stroke study. Brain 128(Pt 5), 1122-1138. doi: 10.1093/brain/awh456
39. Jones, E. G. (1993). GABAergic neurons and their role in cortical plasticity in primates. Cereb. Cortex 3, 361-372. doi: 10.1093/cercor/3.5.361-a
40. Jones, T. A., Allred, R. P., Jefferson, S. C., Kerr, A. L., Woodie, D. A., Cheng, S. Y., et al. (2013). Motor system plasticity in stroke models: intrinsically use-dependent, unreliably useful. Stroke 44(6 Suppl. 1), S104-S106. doi: 10.1161/STR0KEAHA.111.000037
41. Jones, T. A., Chu, C. J., Grande, L. A., and Gregory, A. D. (1999). Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J. Neurosci. 19, 10153-10163.
42. Karni, A., Meyer, G., Rey-Hipolito, C., Jezzard, P., Adams, M. M., Turner, R., et al. (1998). The acquisition of skilled motor performance: fast and slow experience-driven changes in primarymotor cortex. Proc. Natl. Acad. Sci. U.S.A. 95, 861-868. doi: 10.1073/pnas.95.3.861
43. Kerr, A. L., Wolke, M. L., Bell, J. A., and Jones, T. A. (2013). Post-stroke protection from maladaptive effects of learning with the non-paretic forelimb by bimanual home cage experience in C57BL/6 mice. Behav. Brain Res. 252, 180-187. doi: 10.1016/j.bbr.2013.05.062
44. Kleim, J. A., Barbay, S., Cooper, N. R., Hogg, T. M., Reidel, C. N., Remple, M. S., et al. (2002a). Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol. Learn. Mem. 77, 63-77. doi: 10.1006/nlme.2000.4004
45. Kleim, J. A., Freeman, J. H. Jr., Bruneau, R., Nolan, B. C., Cooper, N. R., Zook, A., et al. (2002b). Synapse formation is associated with memory storage in the cerebellum. Proc. Natl. Acad. Sci. U.S.A. 99, 13228-13231. doi: 10.1073/pnas.202483399
46. Kleim, J. A., Barbay, S., and Nudo, R. J. (1998). Functional reorganization of the rat motor cortex following motor skill learning. J. Neurophysiol. 80, 3321-3325.
47. Kleim, J. A., Hogg, T. M., VandenBerg, P. M., Cooper, N. R., Bruneau, R., and Remple, M. (2004). Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J. Neurosci. 24, 628-633. doi: 10.1523/JNEUR0SCI.3440-03.2004
48. Knapp, H. D., Taub, E., and Berman, A. J. (1963). Movements in monkeys with deafferented forelimbs. Exp. Neurol. 7, 305-315. doi: 10.1016/0014-4886(63)90077-3
49. Kozlowski, D. A., James, D. C., and Schallert, T. (1996). Use-dependent exaggeration of neuronal injury after unilateral sensorimotor cortex lesions. J. Neurosci. 16, 4776-4786.
50. Lashley, K. S. (1930). Basic neural mechanisms in behavior. Physiol. Rev. 37, 1-24.
51. Lee, Y. S., Lin, C. Y., Robertson, R. T., Hsiao, I., and Lin, V. W. (2004). Motor recovery and anatomical evidence of axonal regrowth in spinal cord-repaired adult rats. J. Neuropathol. Exp. Neurol. 63, 233-245.
52. Lemon, R. N., and Griffiths, J. (2005). Comparing the function of the corticospinal system in different species: organizational differences for motor specialization? Muscle Nerve 32, 261-279. doi: 10.1002/mus.20333
53. Liepert, J., Graef, S., Uhde, I., Leidner, O., and Weiller, C. (2000). Training-induced changes of motor cortex representations in stroke patients. Acta Neurol. Scand. 101, 321-326. doi: 10.1034/j.1600-0404.2000.90337a.x
54. Liepert, J., Miltner, W. H., Bauder, H., Sommer, M., Dettmers, C., Taub, E., et al. (1998). Motor cortex plasticity during constraint-induced movement therapyin stroke patients. Neurosci. Lett. 250, 5-8. doi: 10.1016/S0304-3940(98)00386-3
55. Liu, R. R., and Murphy, T. H. (2009). Reversible cyclosporin A-sensitive mitochondrial depolarization occurs within minutes of stroke onset in mouse somatosensory cortex in vivo: a two-photon imaging study. J. Biol. Chem. 284, 36109-36117. doi: 10.1074/jbc.M109.055301
56. Liu, Y., and Rouiller, E. M. (1999). Mechanisms of recovery of dexterity following unilateral lesion of the sensorimotor cortex in adult monkeys. Exp. Brain Res. 128, 149-159. doi: 10.1007/S002210050830
57. Loubinoux, I., Carel, C., Pariente, J., Dechaumont, S., Albucher, J. F., Marque, P., et al. (2003). Correlation between cerebral reorganization and motor recovery after subcortical infarcts. Neuroimage 20, 2166-2180. doi: 10.1016/j.neuroimage.2003.08.017
58. Matsuda, F., Sakakima, H., and Yoshida, Y. (2011). The effects of early exercise on brain damage and recovery after focal cerebral infarction in rats. Acta Physiol. 201, 275-287. doi: 10.1111/j.1748-1708.2010.02174.x
59. Milliken, G. W., Plautz, E. J., andNudo, R. J. (2013). Distal forelimb representations in primary motor cortex are redistributed after forelimb restriction: a longitudinal study in adult squirrel monkeys. J. Neurophysiol. 109, 1268-1282. doi: 10.1152/jn.00044.2012
60. Miyai, I., Suzuki, T., Kang, J., Kubota, K., and Volpe, B. T. (1999). Middle cerebral artery stroke that includes the premotor cortex reduces mobility outcome. Stroke 30, 1380-1383. doi: 10.1161/01.STR.30.7.1380
61. Miyai, I., Yagura, H., Hatakenaka, M., Oda, I., Konishi, I., and Kubota, K. (2003). Longitudinal optical imaging study for locomotor recovery after stroke. Stroke 34, 2866-2870. doi: 10.1161/01.STR.0000100166.81077.8A
62. Mohajerani, M. H., Aminoltejari, K., and Murphy, T. H. (2011). Targeted ministrokes produce changes in interhemispheric sensory signal processing that are indicative of disinhibition within minutes. Proc. Natl. Acad. Sci. U.S.A. 108, E183-E191. doi: 10.1073/pnas.1101914108
63. Monfils, M. H., Plautz, E. J., and Kleim, J. A. (2005). In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience. Neuroscientist 11, 471-483. doi: 10.1177/1073858405 278015
64. Murphy, T. H., and Corbett, D. (2009). Plasticity during stroke recovery: from synapse to behaviour. Nat. Rev. Neurosci. 10, 861-872. doi: 10.1038/nrn2735
65. Murphy, T. H., Li, P., Betts, K., and Liu, R. (2008). Two-photon imaging of stroke onset in vivo reveals that NMDA-receptor independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J. Neurosci. 28, 1756-1772. doi: 10.1523/JNEUROSCI.5128-07.2008
66. Napieralski, J. A., Butler, A. K., and Chesselet, M. F. (1996). Anatomical and functional evidence for lesion-specific sprouting of corticostriatal input in the adult rat. J. Comp. Neurol. 373, 484-497. doi: 10.1002/(SICI)1096- 9861(19960930)373:4<484::AID-CNE2>3.0.C0;2-Y
67. Nelles, G., Spiekermann, G., Jueptner, M., Leonhardt, G., Muller, S., Gerhard, H., et al. (1999). Reorganization of sensoryand motor systems in hemiplegic stroke patients. A positron emission tomography study. Stroke 30, 1510-1516. doi: 10.1161/01.STR.30.8.1510
68. Nishibe, M., Barbay, S., Guggenmos, D., and Nudo, R. J. (2010). Reorganization of motor cortex after controlled cortical impact in rats and implications for functional recovery. J. Neurotrauma 27, 2221-2232. doi: 10.1089/neu.2010.1456
69. Nudo, R. J., Jenkins, W. M., Merzenich, M. M., Prejean, T., and Grenda, R. (1992). Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys. J. Neurosci. 12, 2918-2947.
70. Nudo, R. J., and Milliken, G. W. (1996). Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J. Neurophysiol. 75, 2144-2149.
71. Nudo, R. J., Milliken, G. W., Jenkins, W. M., and Merzenich, M. M. (1996a). Use- dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J. Neurosci. 16, 785-807.
72. Nudo, R. J., Wise, B. M., SiFuentes, F., and Milliken, G. W. (1996b). Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272, 1791-1794.
73. Plautz, E. J., Milliken, G. W., and Nudo, R. J. (2000). Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol. Learn. Mem. 74,27-55. doi: 10.1006/nlme.1999.3934
74. Recanzone, G. H., Merzenich, M. M., and Dinse, H. R. (1992). Expansion of the cortical representation of a specific skin field in primary somatosensory cortex by intracortical microstimulation. Cereb. Cortex 2, 181-196. doi: 10.1093/cer- cor/2.3.181
75. Redecker, C., Luhmann, H. J., Hagemann, G., Fritschy, J. M., and Witte, O. W. (2000). Differential downregulation of GABAA receptor subunits in widespread brain regions in the freeze-lesion model of focal cortical malformations. J. Neurosci. 20, 5045-5053.
76. Remple, M. S., Bruneau, R. M., VandenBerg, P. M., Goertzen, C., and Kleim, J. A. (2001). Sensitivity of cortical movement representations to motor experience: evidence that skill learning but not strength training induces cortical reorganization. Behav. Brain Res. 123, 133-141. doi: 10.1016/S0166-4328(01)00199-1
77. Rioult-Pedotti, M. S., Friedman, D., Hess, G., and Donoghue, J. P. (1998). Strengthening of horizontal cortical connections following skill learning. Nat. Neurosci. 1,230-234. doi: 10.1038/678
78. Seitz, R. J., Kleiser, R., and Butefisch, C. M. (2005). Reorganization of cerebral circuits in human brain lesion. Acta Neurochir. Suppl. 93, 65-70. doi: 10.1007/3-211-27577-0-9
79. Sigler, A., and Murphy, T. H. (2010). In vivo 2-photon imaging of fine structure in the rodent brain: before, during, and after stroke. Stroke 41(10 Suppl.), S117-S123. doi: 10.1161/STROKEAHA.110.594648
80. Stroemer, R. P., Kent, T. A., and Hulsebosch, C. E. (1995). Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke 26,2135-2144. doi: 10.1161/01.STR.26.11.2135
81. Stroemer, R. P., Kent, T. A., and Hulsebosch, C. E. (1998). Enhanced neo- cortical neural sprouting, synaptogenesis, and behavioral recovery with D-amphetamine therapy after neocortical infarction in rats. Stroke 29, 2381-2393. discussion: 2393-2385.
82. Taub, E. (1977). Movement in nonhuman primates deprived of somatosensory feedback. Exerc. Sport Sci. Rev. 4, 335-374.
83. Taub, E., Crago, J. E., and Uswatte, G. (1998). Constraint-Induced (CI) Therapy: a new approach to treatment in physical rehabilitation. Rehabil. Psychol. 43, 152-170. doi: 10.1037/0090-5550.43.2.152
84. Teasell, R., Bayona, N. A., and Bitensky, J. (2005). Plasticity and reorganization of the brain post stroke. Top. Stroke Rehabil. 12, 11-26. doi: 10.1310/6AUM-ETYW-Q8XV- 8XAC
85. Traversa, R., Cicinelli, P., Bassi, A., Rossini, P. M., and Bernardi, G. (1997). Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses. Stroke 28, 110-117. doi: 10.1161/01.STR.28.1.110
86. Uesaka, N., Ruthazer, E. S., and Yamamoto, N. (2006). The role of neural activity in cortical axon branching. Neuroscientist 12, 102-106. doi: 10.1177/1073858405281673
87. Ungerleider, L. G., Doyon, J., and Karni, A. (2002). Imaging brain plasticity during motor skill learning. Neurobiol. Learn. Mem. 78, 553-564. doi: 10.1006/nlme.2002.4091
88. Urban, E. T. 3rd., Bury, S. D., Barbay, H. S., Guggenmos, D. J., Dong, Y., and Nudo, R. J. (2012). Gene expression changes of interconnected spared cortical neurons 7 days after ischemic infarct of the primary motor cortex in the rat. Mol. Cell. Biochem. 369, 267-286. doi: 10.1007/s11010-012-1390-z
89. Wang, L., Conner, J. M., Rickert, J., and Tuszynski, M. H. (2011). Structural plasticity within highly specific neuronal populations identifies a unique par- cellation of motor learning in the adult brain. Proc. Natl. Acad. Sci. U.S.A. 108, 2545-2550. doi: 10.1073/pnas.1014335108
90. Wei, L., Erinjeri, J. P., Rovainen, C. M., and Woolsey, T. A. (2001). Collateral growth and angiogenesis around cortical stroke. Stroke 32, 2179-2184. doi: 10.1161/hs0901.094282
91. Weiller, C., Chollet, F., Friston, K. J., Wise, R. J., and Frackowiak, R. S. (1992). Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann. Neurol. 31, 463-472. doi: 10.1002/ana.410310502
92. Weiller, C., Ramsay, S. C., Wise, R. J., Friston, K. J., and Frackowiak, R. S. (1993). Individual patterns of functional reorganization in the human cerebral cortexafter capsular infarction. Ann. Neurol. 33, 181-189. doi: 10.1002/ana.410330208
93. Whishaw, I. Q., Pellis, S. M., Gorny, B. P., and Pellis, V. C. (1991). The impairments in reaching and the movements of compensation in rats with motor cortex lesions: an endpoint, videorecording, and movement notation analysis. Behav. Brain Res. 42, 77-91. doi: 10.1016/S0166-4328(05)80042-7
94. Witte, O. W., and Stoll, G. (1997). Delayed and remote effects of focal cortical infarctions: secondary damage and reactive plasticity. Adv. Neurol. 73, 207-227.
95. Wolf, S. L., Winstein, C. J., Miller, J. P., Taub, E., Uswatte, G., Morris, D., et al. (2006). Effect of constraint-induced movement therapy on upper extremity function 3to9 months after stroke: the EXCITErandomizedclinical trial. JAMA 296, 2095-2104. doi: 10.1001/jama.296.17.2095
96. Woodlee, M. T., and Schallert, T. (2004). The interplay between behavior and neurodegeneration in rat models of Parkinson's disease and stroke. Restor. Neurol. Neurosci. 22, 153-161.
97. Xu, T., Yu, X., Perlik, A. J., Tobin, W. F., Zweig, J. A., Tennant, K., et al. (2009). Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462, 915-919. doi: 10.1038/nature08389
98. Zanette, G., Manganotti, P., Fiaschi, A., and Tamburin, S. (2004). Modulation of motor cortex excitability after upper limb immobilization. Clin. Neurophysiol. 115, 1264-1275. doi: 10.1016/j.clinph.2003.12.033
99. Zhang, S., Boyd, J., Delaney, K., and Murphy, T. H. (2005). Rapid reversible changes in dendritic spine structure in vivo gated by the degree of ischemia. J. Neurosci. 25, 5333-5338. doi: 10.1523/JNEUROSCI.1085-05.2005
100. Zhang, S., and Murphy, T. H. (2007). Imaging the impact of cortical microcirculation on synaptic structure and sensory-evoked hemodynamic responses in vivo. PLoS Biol. 5:e119. doi: 10.1371/journal.pbio.0050119