Thinking outside the brain: Structural plasticity in the spinal cord promotes recovery from cortical stroke

Experimental Neurology

Volumn 254, Issue , 2014, Pages 195-199

  Tennant, Kelly A ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CYTOKINES; MALE; NERVE GROWTH FACTORS; NEURONAL PLASTICITY; RECOVERY OF FUNCTION; SPINAL CORD; STROKE;

EID: 84894058356     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.02.003     Document Type: Note

References (117)

1. Abo M., Chen Z., Lai L.J., Reese T., Bjelke B. Functional recovery after brain lesion-contralateral neuromodulation: an fMRI study. Neuroreport 2001, 12:1543-1547.
2. Adkins D.L., Voorhies A.C., Jones T.A. Behavioral and neuroplastic effects of focal endothelin-1 induced sensorimotor cortex lesions. Neuroscience 2004, 128:473-486.
3. Adkins D.L., Boychuk J., Remple M.S., Kleim J.A. Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J. Appl. Physiol. 2006, 101:1776-1782.
4. Alilain W.J., Horn K.P., Hu H., Dick T.E., Silver J. Functional regeneration of respiratory pathways after spinal cord injury. Nature 2011, 475:196-200.
5. Barrette B., Vallières N., Dubé M., Lacroix S. Expression profile of receptors for myelin-associated inhibitors of axonal regeneration in the intact and injured mouse central nervous system. Mol. Cell. Neurosci. 2007, 34:519-538.
6. Barritt A.W., Davies M., Marchand F., Hartley R., Grist J., Yip P., McMahon S.B., Bradbury E.J. Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J. Neurosci. 2006, 26:10856-10867.
7. Benowitz L.I., Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 1997, 20:84-91.
8. Bestmann S., Swayne O., Blankenburg F., Ruff C.C., Teo J., Weiskopf N., Driver J., Rothwell J.C., Ward N.S. The role of contralesional dorsal premotor cortex after stroke as studied with concurrent TMS-fMRI. J. Neurosci. 2010, 30:11926-11937.
9. Biernaskie J., Szymanska A., Windle V., Corbett D. Bi-hemispheric contribution to functional motor recovery of the affected forelimb following focal ischemic brain injury in rats. Eur. J. Neurosci. 2005, 21:989-999.
10. Bomze H.M., Bulsara K.R., Iskandar B.J., Caroni P., Skene J.H. Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons. Nat. Neurosci. 2001, 4:38-43.
11. Bradbury E.J., Khemani S., Von R., King, Priestley J.V., McMahon S.B. Eur. J. Neurosci. 1999, 11:3873-3883.
12. Bradbury E.J., Moon L.D., Popat R.J., King V.R., Bennett G.S., Patel P.N., Fawcett J.W., McMahon S.B. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002, 416:636-640.
13. Bregman B.S., McAtee M., Dai H.N., Kuhn P.L. Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp. Neurol. 1997, 148:475-494.
14. Brown C.E., Murphy T.H. Livin' on the edge: imaging dendritic spine turnover in the peri-infarct zone during ischemic stroke and recovery. Neuroscientist 2008, 14:139-146.
15. Brown C.E., Li P., Boyd J.D., Delaney K.R., Murphy T.H. Extensive turnover of dendritic spines and vascular remodeling in cortical tissues recovering from stroke. J. Neurosci. 2007, 27:4101-4109.
16. Brown C.E., Wong C., Murphy T.H. Rapid morphologic plasticity of peri-infarct dendritic spines after focal ischemic stroke. Stroke 2008, 39:1286-1291.
17. Brown C.E., Aminoltejari K., Erb H., Winship I.R., Murphy T.H. In vivo voltage-sensitive dye imaging in adult mice reveals that somatosensory maps lost to stroke are replaced over weeks by new structural and functional circuits with prolonged modes of activation within both the peri-infarct zone and distant sites. J. Neurosci. 2009, 29:1719-1734.
18. Brown C.E., Boyd J.D., Murphy T.H. Longitudinal in vivo imaging reveals balanced and branch-specific remodeling of mature cortical pyramidal dendritic arbors after stroke. J. Cereb. Blood Flow Metab. 2010, 30:783-791.
19. Buss A., Sellhaus B., Wolmsley A., Noth J., Schwab M.E., Brook G.A. Expression pattern of NOGO-A protein in the human nervous system. Acta Neuropathol. 2005, 110:113-119.
20. Cafferty W.B., Bradbury E.J., Lidierth M., Jones M., Duffy P.J., Pezet S., McMahon S.B. Chondroitinase ABC-mediated plasticity of spinal sensory function. J. Neurosci. 2008, 28:11998-12009.
21. Calautti C., Jones P.S., Naccarato M., Sharma N., Day D.J., Bullmore E.T., Warburton E.A., Baron J.C. The relationship between motor deficit and primary motor cortex hemispheric activation balance after stroke: longitudinal fMRI study. J. Neurol. Neurosurg. Psychiatry 2010, 81:788-792.
22. Cao Y., George K.P., Ewing J.R., Vikingstad E.M., Johnson A.F. Neuroimaging of language and aphasia after stroke. J. Stroke Cerebrovasc. Dis. 1998, 7:230-233.
23. Carmichael S.T. Targets for neural repair therapies after stroke. Stroke 2010, 41:S124-S126.
24. Carmichael S.T., Chesselet M.F. Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. J. Neurosci. 2002, 22:6062-6070.
25. Carmichael S.T., Wei L., Rovainen C.M., Woolsey T.A. New patterns of intracortical projections after focal cortical stroke. Neurobiol. Dis. 2001, 8:910-922.
26. Carmichael S.T., Archibeque I., Luke L., Nolan T., Momiy J., Li S. Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Exp. Neurol. 2005, 193:291-311.
27. Castro-Alamancos M.A., Borrel J. Functional recovery of forelimb response capacity after forelimb primary motor cortex damage in the rat is due to the reorganization of adjacent areas of cortex. Neuroscience 1995, 68:793-805.
28. Chen M.S., Huber A.B., van der Haar M.E., Frank M., Schnell L., Spillmann A.A., Christ F., Schwab M.E. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 2000, 403:434-439.
29. Chen J., Li Y., Wang L., Lu M., Chopp M. Caspase inhibition by Z-VAD increases the survival of grafted bone marrow cells and improves functional outcome after MCAo in rats. J. Neurol. Sci. 2002, 199:17-24.
30. Chollet F., DiPiero V., Wise R.J., Brooks D.J., Dolan R.J., Frackowiak R.S. The functional anatomy of motor recovery after stroke in humans: a study with positron emission tomography. Ann. Neurol. 1991, 29:63-71.
31. Cicinelli P., Traversa R., Rossini P.M. Post-stroke reorganization of brain motor output to the hand: a 2-4month follow-up with focal magnetic transcranial stimulation. Electroencephalogr. Clin. Neurophysiol. 1997, 105:438-450.
32. Dancause N. Vicarious function of remote cortex following stroke: recent evidence from human and animal studies. Neuroscientist 2006, 12:489-499.
33. Dancause N., Barbay S., Frost S.B., Plautz E.J., Chen D., Zoubina E.V., Stowe A.M., Nudo R.J. Extensive cortical rewiring after brain injury. J. Neurosci. 2005, 25:10167-10179.
34. Di Giovanni S., Knoblach S.M., Brandoli C., Aden S.A., Hoffman E.P., Faden A.I. Gene profiling in spinal cord injury shows role of cell cycle in neuronal death. Ann. Neurol. 2003, 53:454-468.
35. Dijkhuizen R.M., Ren J., Mandeville J.B., Wu O., Ozdag F.M., Moskowitz M.A., Rosen B.R., Finklestein S.P. Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12766-12771.
36. Dijkhuizen R.M., Singhal A.B., Mandeville J.B., Wu O., Halpern E.F., Finklestein S.P., Rosen B.R., Lo E.H. Correlation between brain reorganization, ischemic damage, and neurologic status after transient focal cerebral ischemia in rats: a functional magnetic resonance imaging study. J. Neurosci. 2003, 23:510-517.
37. Fouad K., Klusman I., Schwab M.E. Regenerating corticospinal fibers in the Marmoset (Callitrix jacchus) after spinal cord lesion and treatment with the anti-Nogo-A antibody IN-1. Eur. J. Neurosci. 2004, 20:2479-2482.
38. Freund P., Schmidlin E., Wannier T., Bloch J., Mir A., Schwab M.E., Rouiller E.M. Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat. Med. 2006, 12:790-792.
39. Freund P., Wannier T., Schmidlin E., Bloch J., Mir A., Schwab M.E., Rouiller E.M. Anti-Nogo-A antibody treatment enhances sprouting of corticospinal axons rostral to a unilateral cervical spinal cord lesion in adult macaque monkey. J. Comp. Neurol. 2007, 502:644-659.
40. Fridman E.A., Hanakawa T., Chung M., Hummel F., Leiguarda R.C., Cohen L.G. Reorganization of the human ipsilesional premotor cortex after stroke. Brain 2004, 127:747-758.
41. Friel K.M., Heddings A.A., Nudo R.J. Effects of postlesion experience on behavioral recovery and neurophysiologic reorganization after cortical injury in primates. Neurorehabil. Neural Repair 2000, 14:187-198.
42. Frost S.B., Barbay S., Friel K.M., Plautz E.J., Nudo R.J. Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J. Neurophysiol. 2003, 89:3205-3214.
43. Galtrey C.M., Asher R.A., Nothias F., Fawcett J.W. Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain 2007, 130:926-939.
44. García-Alías G., Barkhuysen S., Buckle M., Fawcett J.W. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat. Neurosci. 2009, 12:1145-1151.
45. Gharbawie O.A., Gonzalez C.L., Williams P.T., Kleim J.A., Whishaw I.Q. Middle cerebral artery (MCA) stroke produces dysfunction in adjacent motor cortex as detected by intracortical microstimulation in rats. Neuroscience 2005, 130:601-610.
46. GrandPré T., Nakamura F., Vartanian T., Strittmatter S.M. Identification of the Nogo inhibitor of axon regeneration as a reticulon protein. Nature 2000, 403:439-444.
47. Grill R., Murai K., Blesch A., Gage F.H., Tuszynski M.H. Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J. Neurosci. 1997, 17:5560-5572.
48. Hakkoum D., Stoppini L., Muller D. Interleukin-6 promotes sprouting and functional recovery in lesioned organotypic hippocampal slice cultures. J. Neurochem. 2007, 100:747-757.
49. Hammond E.N., Tetzlaff W., Mestres P., Giehl K.M. BDNF, but not NT-3, promotes long-term survival of axotomized adult rat corticospinal neurons in vivo. Neuroreport 1999, 10:2671-2675.
50. Hayashi M., Ueyama T., Nemoto K., Tamaki T., Senba E. Sequential mRNA expression for immediate early genes, cytokines, and neurotrophins in spinal cord injury. J. Neurotrauma 2000, 17:203-218.
51. Ho C., Tessier-Lavigne M. Challenges to the report of Nogo antibody effects in primates. Nat. Med. 2006, 1232. (author reply 1232-1233).
52. Hoffman P.N. Expression of GAP-43, a rapidly transported growth-associated protein, and class II beta tubulin, a slowly transported cytoskeletal protein, are coordinated in regenerating neurons. J. Neurosci. 1989, 9:893-897.
53. Hsu J.E., Jones T.A. Contralesional neural plasticity and functional changes in the less-affected forelimb after large and small cortical infarcts in rats. Exp. Neurol. 2006, 201:479-494.
54. Huber A.B., Schwab M.E. Nogo-A, a potent inhibitor of neurite outgrowth and regeneration. Biol. Chem. 2000, 381:407-419.
55. Hunanyan A.S., García-Alías G., Alessi V., Levine J.M., Fawcett J.W., Mendell L.M., Arvanian V.L. Role of chondroitin sulfate proteoglycans in axonal conduction in mammalian spinal cord. J. Neurosci. 2010, 30:7761-7769.
56. Johansen-Berg H., Dawes H., Guy C., Smith S.M., Wade D.T., Matthews P.M. Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. Brain 2002, 125:2731-2742.
57. Johansen-Berg H., Rushworth M.F., Bogdanovic M.D., Kischka U., Wimalaratna S., Matthews P.M. The role of ipsilateral premotor cortex in hand movement after stroke. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:14518-14523.
58. Kawamata T., Dietrich W.D., Schallert T., Gotts J.E., Cocke R.R., Benowitz L.I., Finklestein S.P. Intracisternal basic fibroblast growth factor enhances functional recovery and up-regulates the expression of a molecular marker of neuronal sprouting following focal cerebral infarction. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:8179-8184.
59. Kleim J.A., Barbay S., Nudo R.J. Functional reorganization of the rat motor cortex following motor skill learning. J. Neurophysiol. 1998, 80:3321-3325.
60. Kleim J.A., Bruneau R., VandenBerg P., MacDonald E., Mulrooney R., Pocock D. Motor cortex stimulation enhances motor recovery and reduces peri-infarct dysfunction following ischemic insult. Neurol. Res. 2003, 25:789-793.
61. Kumar P., Moon L.D. Therapeutics targeting Nogo-A hold promise for stroke restoration. CNS Neurol. Disord. Drug Targets 2013, 12:200-208.
62. Lapash Daniels C.M., Ayers K.L., Finley A.M., Culver J.P., Goldberg M.P. Axon sprouting in adult mouse spinal cord after motor cortex stroke. Neurosci. Lett. 2009, 450:191-195.
63. Lee J.K., Kim J.E., Sivula M., Strittmatter S.M. Nogo receptor antagonism promotes stroke recovery by enhancing axonal plasticity. J. Neurosci. 2004, 24:6209-6217.
64. Leu B., Koch E., Schmidt J.T. GAP43 phosphorylation is critical for growth and branching of retinotectal arbors in zebrafish. Dev. Neurobiol. 2010, 70:897-911.
65. Li S., Carmichael S.T. Growth-associated gene and protein expression in the region of axonal sprouting in the aged brain after stroke. Neurobiol. Dis. 2006, 23:362-373.
66. Li P., Murphy T.H. Two-photon imaging during prolonged middle cerebral artery occlusion in mice reveals recovery of dendritic structure after reperfusion. J. Neurosci. 2008, 28:11970-11979.
67. Li Y., Jiang N., Powers C., Chopp M. Neuronal damage and plasticity identified by microtubule-associated protein 2, growth-associated protein 43, and cyclin D1 immunoreactivity after focal cerebral ischemia in rats. Stroke 1998, 29:1972-1980. (discussion 1980-1971).
68. Liu Z., Li Y., Qu R., Shen L., Gao Q., Zhang X., Lu M., Savant-Bhonsale S., Borneman J., Chopp M. Axonal sprouting into the denervated spinal cord and synaptic and postsynaptic protein expression in the spinal cord after transplantation of bone marrow stromal cell in stroke rats. Brain Res. 2007, 1149:172-180.
69. Liu Z., Li Y., Zhang X., Savant-Bhonsale S., Chopp M. Contralesional axonal remodeling of the corticospinal system in adult rats after stroke and bone marrow stromal cell treatment. Stroke 2008, 39:2571-2577.
70. Liu Z., Zhang R.L., Li Y., Cui Y., Chopp M. Remodeling of the corticospinal innervation and spontaneous behavioral recovery after ischemic stroke in adult mice. Stroke 2009, 40:2546-2551.
71. Liu Z., Li Y., Zhang R.L., Cui Y., Chopp M. Bone marrow stromal cells promote skilled motor recovery and enhance contralesional axonal connections after ischemic stroke in adult mice. Stroke 2011, 42:740-744.
72. Luhmann H.J., Mudrick-Donnon L.A., Mittmann T., Heinemann U. Ischaemia-induced long-term hyperexcitability in rat neocortex. Eur. J. Neurosci. 1995, 7:180-191.
73. Lundell H., Christensen M.S., Barthélemy D., Willerslev-Olsen M., Biering-Sørensen F., Nielsen J.B. Cerebral activation is correlated to regional atrophy of the spinal cord and functional motor disability in spinal cord injured individuals. Neuroimage 2011, 54:1254-1261.
74. Marchetti L., Klein M., Schlett K., Pfizenmaier K., Eisel U.L. Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-d-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J. Biol. Chem. 2004, 279:32869-32881.
75. Massey J.M., Hubscher C.H., Wagoner M.R., Decker J.A., Amps J., Silver J., Onifer S.M. Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J. Neurosci. 2006, 26:4406-4414.
76. Mohajerani M.H., Aminoltejari K., Murphy T.H. Targeted mini-strokes produce changes in interhemispheric sensory signal processing that are indicative of disinhibition within minutes. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:E183-E191.
77. Moon L.D., Asher R.A., Rhodes K.E., Fawcett J.W. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat. Neurosci. 2001, 4:465-466.
78. Motta-Oishi A.A., Magalhães F.H., Mícolis de Azevedo F. Neuromuscular electrical stimulation for stroke rehabilitation: is spinal plasticity a possible mechanism associated with diminished spasticity?. Med. Hypotheses 2013, 81:784-788.
79. Nelson T.E., Olde Engberink A., Hernandez R., Puro A., Huitron-Resendiz S., Hao C., De Graan P.N., Gruol D.L. Altered synaptic transmission in the hippocampus of transgenic mice with enhanced central nervous systems expression of interleukin-6. Brain Behav. Immun. 2012, 26:959-971.
80. Nudo R.J., Milliken G.W. Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J. Neurophysiol. 1996, 75:2144-2149.
81. Oshima T., Lee S., Sato A., Oda S., Hirasawa H., Yamashita T. TNF-alpha contributes to axonal sprouting and functional recovery following traumatic brain injury. Brain Res. 2009, 1290:102-110.
82. Papadopoulos C.M., Tsai S.Y., Alsbiei T., O'Brien T.E., Schwab M.E., Kartje G.L. Functional recovery and neuroanatomical plasticity following middle cerebral artery occlusion and IN-1 antibody treatment in the adult rat. Ann. Neurol. 2002, 51:433-441.
83. Pizzorusso T., Medini P., Landi S., Baldini S., Berardi N., Maffei L. Structural and functional recovery from early monocular deprivation in adult rats. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8517-8522.
84. Prinjha R., Moore S.E., Vinson M., Blake S., Morrow R., Christie G., Michalovich D., Simmons D.L., Walsh F.S. Inhibitor of neurite outgrowth in humans. Nature 2000, 403:383-384.
85. Remple M.S., Bruneau R.M., VandenBerg P.M., Goertzen C., Kleim J.A. Sensitivity of cortical movement representations to motor experience: evidence that skill learning but not strength training induces cortical reorganization. Behav. Brain Res. 2001, 123:133-141.
86. Risher W.C., Ard D., Yuan J., Kirov S.A. Recurrent spontaneous spreading depolarizations facilitate acute dendritic injury in the ischemic penumbra. J. Neurosci. 2010, 30:9859-9868.
87. Rosenzweig E.S., Courtine G., Jindrich D.L., Brock J.H., Ferguson A.R., Strand S.C., Nout Y.S., Roy R.R., Miller D.M., Beattie M.S., Havton L.A., Bresnahan J.C., Edgerton V.R., Tuszynski M.H. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat. Neurosci. 2010, 13:1505-1510.
88. Schnell L., Schneider R., Kolbeck R., Barde Y.A., Schwab M.E. Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 1994, 367:170-173.
89. Schwab M.E. Nogo and axon regeneration. Curr. Opin. Neurobiol. 2004, 14:118-124.
90. Sist B., Fouad K., Winship I.R. Plasticity beyond peri-infarct cortex: spinal up regulation of structural plasticity, neurotrophins, and inflammatory cytokines during recovery from cortical stroke. Exp. Neurol. 2014, 252C:47-56.
91. Soleman S., Yip P.K., Duricki D.A., Moon L.D. Delayed treatment with chondroitinase ABC promotes sensorimotor recovery and plasticity after stroke in aged rats. Brain 2012, 135:1210-1223.
92. Song G., Cechvala C., Resnick D.K., Dempsey R.J., Rao V.L. GeneChip analysis after acute spinal cord injury in rat. J. Neurochem. 2001, 79:804-815.
93. Steward O., Zheng B., Tessier-Lavigne M., Hofstadter M., Sharp K., Yee K.M. Regenerative growth of corticospinal tract axons via the ventral column after spinal cord injury in mice. J. Neurosci. 2008, 28:6836-6847.
94. Stroemer R.P., Kent T.A., Hulsebosch C.E. Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke 1995, 26:2135-2144.
95. Suzuki S., Tanaka K., Suzuki N. Ambivalent aspects of interleukin-6 in cerebral ischemia: inflammatory versus neurotrophic aspects. J. Cereb. Blood Flow Metab. 2009, 29:464-479.
96. Takahashi-Iwanaga H., Murakami T., Abe K. Three-dimensional microanatomy of perineuronal proteoglycan nets enveloping motor neurons in the rat spinal cord. J. Neurocytol. 1998, 27:817-827.
97. Takatsuru Y., Fukumoto D., Yoshitomo M., Nemoto T., Tsukada H., Nabekura J. Neuronal circuit remodeling in the contralateral cortical hemisphere during functional recovery from cerebral infarction. J. Neurosci. 2009, 29:10081-10086.
98. Traversa R., Cicinelli P., Bassi A., Rossini P.M., Bernardi G. Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses. Stroke 1997, 28:110-117.
99. Tsai S.Y., Markus T.M., Andrews E.M., Cheatwood J.L., Emerick A.J., Mir A.K., Schwab M.E., Kartje G.L. Intrathecal treatment with anti-Nogo-A antibody improves functional recovery in adult rats after stroke. Exp. Brain Res. 2007, 182:261-266.
100. Tsai S.Y., Papadopoulos C.M., Schwab M.E., Kartje G.L. Delayed anti-Nogo-A therapy improves function after chronic stroke in adult rats. Stroke 2011, 42:186-190.
101. Turrin N.P., Rivest S. Tumor necrosis factor alpha but not interleukin 1 beta mediates neuroprotection in response to acute nitric oxide excitotoxicity. J. Neurosci. 2006, 26:143-151.
102. Tuszynski M. Challenges to the report of Nogo antibody effects in primates. Nat. Med. 2006, 12:1231-1232. (author reply 1232-1233).
103. Vavrek R., Girgis J., Tetzlaff W., Hiebert G.W., Fouad K. BDNF promotes connections of corticospinal neurons onto spared descending interneurons in spinal cord injured rats. Brain 2006, 129:1534-1545.
104. Wang X., Chun S.J., Treloar H., Vartanian T., Greer C.A., Strittmatter S.M. Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 2002, 22:5505-5515.
105. Weber R., Ramos-Cabrer P., Justicia C., Wiedermann D., Strecker C., Sprenger C., Hoehn M. Early prediction of functional recovery after experimental stroke: functional magnetic resonance imaging, electrophysiology, and behavioral testing in rats. J. Neurosci. 2008, 28:1022-1029.
106. Wei L., Erinjeri J.P., Rovainen C.M., Woolsey T.A. Collateral growth and angiogenesis around cortical stroke. Stroke 2001, 32:2179-2184.
107. Weishaupt N., Silasi G., Colbourne F., Fouad K. Secondary damage in the spinal cord after motor cortex injury in rats. J. Neurotrauma 2010, 27:1387-1397.
108. Wiessner C., Bareyre F.M., Allegrini P.R., Mir A.K., Frentzel S., Zurini M., Schnell L., Oertle T., Schwab M.E. Anti-Nogo-A antibody infusion 24hours after experimental stroke improved behavioral outcome and corticospinal plasticity in normotensive and spontaneously hypertensive rats. J. Cereb. Blood Flow Metab. 2003, 23:154-165.
109. Winship I.R., Murphy T.H. In vivo calcium imaging reveals functional rewiring of single somatosensory neurons after stroke. J. Neurosci. 2008, 28:6592-6606.
110. Winship I.R., Murphy T.H. Remapping the somatosensory cortex after stroke: insight from imaging the synapse to network. Neuroscientist 2009, 15:507-524.
111. Yang P., Wen H., Ou S., Cui J., Fan D. IL-6 promotes regeneration and functional recovery after cortical spinal tract injury by reactivating intrinsic growth program of neurons and enhancing synapse formation. Exp. Neurol. 2012, 236:19-27.
112. Ye J.H., Houle J.D. Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp. Neurol. 1997, 143:70-81.
113. Zagrebelsky M., Buffo A., Skerra A., Schwab M.E., Strata P., Rossi F. Retrograde regulation of growth-associated gene expression in adult rat Purkinje cells by myelin-associated neurite growth inhibitory proteins. J. Neurosci. 1998, 18:7912-7929.
114. Zai L., Ferrari C., Dice C., Subbaiah S., Havton L.A., Coppola G., Geschwind D., Irwin N., Huebner E., Strittmatter S.M., Benowitz L.I. Inosine augments the effects of a Nogo receptor blocker and of environmental enrichment to restore skilled forelimb use after stroke. J. Neurosci. 2011, 31:5977-5988.
115. Zhang S., Murphy T.H. Imaging the impact of cortical microcirculation on synaptic structure and sensory-evoked hemodynamic responses in vivo. PLoS Biol. 2007, 5:e119.
116. Zhang Y., Xiong Y., Mahmood A., Meng Y., Liu Z., Qu C., Chopp M. Sprouting of corticospinal tract axons from the contralateral hemisphere into the denervated side of the spinal cord is associated with functional recovery in adult rat after traumatic brain injury and erythropoietin treatment. Brain Res. 2010, 1353:249-257.
117. Zuber M.X., Goodman D.W., Karns L.R., Fishman M.C. The neuronal growth-associated protein GAP-43 induces filopodia in non-neuronal cells. Science 1989, 244:1193-1195.