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  • Print publication year: 2014
  • Online publication date: May 2014

Chapter 12 - The role of extracellular matrix in plasticity in the spinal cord

from Section 3 - Plasticity after injury to the central nervous system

References

1. RossignolS, SchwabM, SchwartzM, et al. Spinal cord injury: time to move? J Neurosci 2007; 27: 11782–92.
2. HulseboschCE. Recent advances in pathophysiology and treatment of spinal cord injury. Adv Physiol Educ 2002; 26: 238–55.
3. FawcettJW, CurtA, SteevesJD, et al. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: spontaneous recovery after spinal cord injury and statistical power needed for therapeutic clinical trials. Spinal Cord 2007; 45: 190–205.
4. SteevesJD, KramerJK, FawcettJW, et al. Extent of spontaneous motor recovery after traumatic cervical sensorimotor complete spinal cord injury. Spinal Cord 2011; 49: 257–65.
5. SadowskyCL, McDonaldJW. Activity-based restorative therapies: concepts and applications in spinal cord injury-related neurorehabilitation. Dev Disabil Res Rev 2009; 15: 112–16.
6. BarbeauH, NormanK, FungJ, et al. Does neurorehabilitation play a role in the recovery of walking in neurological populations? Ann N Y Acad Sci 1998; 860: 377–92.
7. Garcia-AliasG, BarkhuysenS, BuckleM, et al. Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 2009; 12: 1145–51.
8. MatthewsRT, KellyGM, ZerilloCA, et al. Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J Neurosci 2002; 22: 7536–47.
9. GaltreyCM, FawcettJW. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res Rev 2007; 54: 1–18.
10. HenschTK. Critical period regulation. Annu Rev Neurosci 2004; 27: 549–79.
11. DeepaSS, CarulliD, GaltreyC, et al. Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J Biol Chem 2006; 281: 17789–800.
12. KwokJC, AfshariF, García-AlíasG, et al. Proteoglycans in the central nervous system: plasticity, regeneration and their stimulation with chondroitinase ABC. Restor Neurol Neurosci 2008; 26: 131–45.
13. AsherRA, MorgensternDA, FidlerPS, et al. Neurocan is up-regulated in injured brain and in cytokine-treated astrocytes. J Neurosci 2000; 20: 2427–38.
14. AsherRA, ScheibeRJ, KeiserHD, et al. On the existence of a cartilage-like proteoglycan and link proteins in the central nervous system. Glia 1995; 13: 294–308.
15. EngelM, MaurelP, MargolisRU, et al. Chondroitin sulfate proteoglycans in the developing central nervous system. I. Cellular sites of synthesis of neurocan and phosphacan. J Comp Neurol 1996; 366: 34–43.
16. SeidenbecherCI, GundelfingerED, BöckersTM, et al. Transcripts for secreted and GPI-anchored brevican are differentially distributed in rat brain. Eur J Neurosci 1998; 10: 1621–30.
17. YamadaH, FredetteB, ShitaraK, et al. The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons. J Neurosci 1997; 17: 7784–95.
18. YamadaH, WatanabeK, ShimonakaM, et al. Molecular cloning of brevican, a novel brain proteoglycan of the aggrecan/versican family. J Biol Chem 1994; 269: 10119–26.
19. MaurelP, RauchU, FladM, et al. Phosphacan, a chondroitin sulfate proteoglycan of brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of a receptor-type protein tyrosine phosphatase. PNAS 1994; 91: 2512–16.
20. TangX, DaviesJE, DaviesSJ. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphacan, brevican, versican V2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J Neurosci Res 2003; 71: 427–44.
21. JonesLL, YamaguchiY, StallcupWB, et al. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J Neurosci 2002; 22: 2792–803.
22. StallcupWB, BeasleyL. Bipotential glial precursor cells of the optic nerve express the NG2 proteoglycan. J Neurosci 1987; 7: 2737–44.
23. CarulliD, PizzorussoT, KwokJC, et al. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 2010; 133: 2331–2347.
24. DityatevA, SchachnerM. Extracellular matrix molecules and synaptic plasticity. Nat Rev Neurosci 2003; 4: 456–468.
25. BrakebuschC, SeidenbecherCI, AsztelyF, et al. Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol Cell Biol 2002; 22: 7417–27.
26. BukaloO, SchachnerM, DityatevA. Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 2001; 104: 359–69.
27. ZhouXH, BrakebuschC, MatthiesH, et al. Neurocan is dispensable for brain development. Mol Cell Biol 2001; 21: 5970–8.
28. SaghatelyanAK, DityatevA, SchmidtS, et al. Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol Cell Neurosci 2001; 17: 226–40.
29. NikonenkoA, SchmidtS, SkiboG, et al. Tenascin-R-deficient mice show structural alterations of symmetric perisomatic synapses in the CA1 region of the hippocampus. J Comp Neurol 2003; 456: 338–49.
30. MorelliniF, SivukhinaE, StoenicaL, et al. Improved reversal learning and working memory and enhanced reactivity to novelty in mice with enhanced GABAergic innervation in the dentate gyrus. Cereb Cortex 2010; 20: 2712–27.
31. PasterkampRJ, GigerRJ. Semaphorin function in neural plasticity and disease. Curr Opin Neurobiol 2009; 19: 263–74.
32. PasterkampRJ, VerhaagenJ. Semaphorins in axon regeneration: developmental guidance molecules gone wrong? Philos Trans R Soc Lond B Biol Sci 2006; 361: 1499–511.
33. SchultzeW, EulenburgV, LessmannV, et al. Semaphorin 4F interacts with the synapse-associated protein P90/PSD-95. J Neurochem 2001; 783: 482–9.
34. InagakiS, OhokaY, SugimotoH, et al. Sema4c, a transmembrane semaphorin, interacts with a post-synaptic density protein, PSD-95. J Biol Chem 2001; 276: 9174–81.
35. KüryP, AbankwaD, KruseF, et al. Gene expression profiling reveals multiple novel intrinsic and extrinsic factors associated with axonal regeneration failure. Eur J Neurosci 2004; 19: 32–42.
36. Moreau-FauvarqueC, KumanogohA, CamandE, et al. The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and up-regulated after CNS lesion. J Neurosci 2003; 23: 9229–39.
37. PasterkampRJ, KolkSM, HellemonsAJ, et al. Expression patterns of semaphorin7A and plexinC1 during rat neural development suggest roles in axon guidance and neuronal migration. BMC Dev Biol 2007; 7: 98.
38. ShiomiT, LemaîtreV, D’ArmientoJ, et al. Matrix metalloproteinases, a disintegrin and metalloproteinases, and a disintegrin and metalloproteinases with thrombospondin motifs in non-neoplastic diseases. Pathol Int 2010; 60: 477–96.
39. AgrawalSM, LauL, YongVW. MMPs in the central nervous system: where the good guys go bad. Semin Cell Dev Biol 2008; 19: 42–51.
40. AnthonyDC, FergusonB, MatyzakMK, et al. Differential matrix metalloproteinase expression in cases of multiple sclerosis and stroke. Neuropathol Appl Neurobiol 1997; 23: 406–15.
41. BussA, PechK, KakulasBA, et al. Matrix metalloproteinases and their inhibitors in human traumatic spinal cord injury. BMC Neurol 2007; 7: 17.
42. MeighanSE, MeighanPC, ChoudhuryP, et al. Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J Neurochem 2006; 96: 1227–41.
43. NagyV, BozdagiO, MatyniaA, et al. Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J Neurosci 2006; 26: 1923–34.
44. SilverJ, MillerJH. Regeneration beyond the glial scar. Nat Rev Neurosci 2004; 5: 146–56.
45. PrestonE, WebsterJ, SmallD. Characteristics of sustained blood–brain barrier opening and tissue injury in a model for focal trauma in the rat. J Neurotrauma 2001; 18: 83–92.
46. FawcettJW, AsherRA. The glial scar and central nervous system repair. Brain Res Bull 1999; l49: 377–91.
47. RollsA, ShechterR, SchwartzM. The bright side of the glial scar in CNS repair. Nat Rev Neurosci 2009; 10: 235–41.
48. BushTG, PuvanachandraN, HornerCH, et al. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 1999; 23: 297–308.
49. FaulknerJR, HerrmannJE, WooMJ, et al. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 2004; 24: 2143–55.
50. HobohmC, GüntherA, GroscheJ, et al. Decomposition and long-lasting downregulation of extracellular matrix in perineuronal nets induced by focal cerebral ischemia in rats. J Neurosci Res 2005; 80: 539–48.
51. HarrisNG, MironovaYA, HovdaDA, et al. Pericontusion axon sprouting is spatially and temporally consistent with a growth-permissive environment after traumatic brain injury. J Neuropathol Exp Neurol 2010; 69: 139–54.
52. MasseyJM, HubscherCH, WagonerMR, et al. Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci 2006; 26: 4406–14.
53. ApostolovaI, IrintchevA, SchachnerM. Tenascin-R restricts posttraumatic remodeling of motoneuron innervation and functional recovery after spinal cord injury in adult mice. J Neurosci 2006; 26: 7849–59.
54. DouCL, LevineJM. Inhibition of neurite growth by the NG2 chondroitin sulfate proteoglycan. J Neurosci 1994; 14: 7616–28.
55. FriedlanderDR, MilevP, KarthikeyanL, et al. The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 1994; 125: 669–80.
56. Smith-ThomasL, Fok-SeangJ, StevensJ, et al. An inhibitor of neurite outgrowth produced by astrocytes. J Cell Sci 1994; 107:1687–95.
57. SnowDM, LemmonV, CarrinoDA, et al. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurol 1990; 109: 111–30.
58. Smith-ThomasLC, StevensJ, Fok-SeangJ, et al. Increased axon regeneration in astrocytes grown in the presence of proteoglycan synthesis inhibitors. J Cell Sci 1995; 108: 1307–15.
59. LaabsTL, WangH, KatagiriY, et al. Inhibiting glycosaminoglycan chain polymerization decreases the inhibitory activity of astrocyte-derived chondroitin sulfate proteoglycans. J Neurosci 2007; 27: 14494–501.
60. SnowDM, AtkinsonPB, HassingerTD, et al. Chondroitin sulfate proteoglycan elevates cytoplasmic calcium in DRG neurons. Dev Biol 1994; 166: 87–100.
61. BorisoffJF, ChanCC, HiebertGW, et al. Suppression of Rho-kinase activity promotes axonal growth on inhibitory CNS substrates. Mol Cell Neurosci 2003; 22: 405–16.
62. DerghamP, EllezamB, EssagianC, et al. Rho signaling pathway targeted to promote spinal cord repair. J Neurosci 2002; 22: 6570–7.
63. MonnierPP, SierraA, SchwabJM, et al. The Rho/ROCK pathway mediates neurite growth-inhibitory activity associated with the chondroitin sulfate proteoglycans of the CNS glial scar. Mol Cell Neurosci 2003; 22: 319–30.
64. SivasankaranR, PeiJ, WangKC, et al. PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration. Nat Neurosci 2004; 7: 261–8.
65. KoprivicaV, ChoKS, ParkJB, et al. EGFR activation mediates inhibition of axon regeneration by myelin and chondroitin sulfate proteoglycans. Science 2005; 310: 106–10.
66. ZhouFQ, WalzerM, WuYH, et al. Neurotrophins support regenerative axon assembly over CSPGs by an ECM-integrin-independent mechanism. J Cell Sci 2006; 119: 2787–96.
67. ShenY, TenneyAP, BuschSA, et al. PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 2009; 326: 592–6.
68. WellsJE, RiceTK, NuttallRK, et al. An adverse role for matrix metalloproteinase-12 after spinal cord injury in mice. J Neurosci 2003; 23: 10107–15.
69. HsuJY, BourguignonLY, AdamsCM, et al. Matrix metalloproteinase-9 facilitates glial scar formation in the injured spinal cord. J Neurosci 2008; 28: 13467–77.
70. NobleLJ, DonovanF, IgarashiT, et al. Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J Neurosci 2002; 22: 7526–35.
71. HsuJY, McKeonR, GoussevS, et al. Matrix metalloproteinase-2 facilitates wound healing events that promote functional recovery after spinal cord injury. J Neurosci 2006; 26: 9841–50.
72. TateCC, TateMC, LaPlacaMC. Fibronectin and laminin increase in the mouse brain after controlled cortical impact injury. J Neurotrauma 2007; 24: 226–30.
73. HausmannR, BetzP. The time course of the vascular response to human brain injury–an immunohistochemical study. Int J Legal Med 2000; 113: 288–92.
74. HermannsS, KlapkaN, GasisM, et al. The collagenous wound healing scar in the injured central nervous system inhibits axonal regeneration. Adv Exp Med Biol 2006; 557: 177–90.
75. DavisGE, SengerDR. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res 2005; 97: 1093–107.
76. De WinterF, OudegaM, LankhorstAJ, et al. Injury-induced class 3 semaphorin expression in the rat spinal cord. Exp Neurol 2002; 175: 61–75.
77. WeidnerN, GrillRJ, TuszynskiMH. Elimination of basal lamina and the collagen “scar” after spinal cord injury fails to augment corticospinal tract regeneration. Exp Neurol 1999; 160: 40–50.
78. LiHP, HommaA, SangoK, et al. Regeneration of nigrostriatal dopaminergic axons by degradation of chondroitin sulfate is accompanied by elimination of the fibrotic scar and glia limitans in the lesion site. J Neurosci Res 2007; 85: 536–547.
79. JoesterA, FaissnerA. The structure and function of tenascins in the nervous system. Matrix Biol 2001; 20: 13–22.
80. CelioMR, SpreaficoR, De BiasiS, et al. Perineuronal nets: past and present. Trends Neurosci 1998; 21: 510–15.
81. AndrewsMR, CzvitkovichS, DassieE, et al. Alpha9 integrin promotes neurite outgrowth on tenascin-C and enhances sensory axon regeneration. J Neurosci 2009; 29: 5546–57.
82. ChristophersonKS, UllianEM, StokesCC, et al. Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 2005; 120: 421–33.
83. LiauwJ, HoangS, ChoiM, et al. Thrombospondins 1 and 2 are necessary for synaptic plasticity and functional recovery after stroke. J Cereb Blood Flow Metab 2008; 28: 1722–32.
84. CalancieB, LuttonS, BrotonJG. Central nervous system plasticity after spinal cord injury in man: interlimb reflexes and the influence of cutaneous stimulation. Electroencephalogr Clin Neurophysiol 1996; 101: 304–15.
85. CalancieB, MolanoMR, BrotonJG. Interlimb reflexes and synaptic plasticity become evident months after human spinal cord injury. Brain 2002; 125: 1150–61.
86. DitunnoJF Jr, CohenME, HauckWW, et al. Recovery of upper-extremity strength in complete and incomplete tetraplegia: a multicenter study. Arch Phys Med Rehabil 2000; 81: 389–93.
87. WeidnerN, NerA, SalimiN, et al. Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. PNAS 2001; 98: 3513–8.
88. BareyreFM, KerschensteinerM, RaineteauO, et al. The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 2004; 7: 269–77.
89. BallermannM, FouadK. Spontaneous locomotor recovery in spinal cord injured rats is accompanied by anatomical plasticity of reticulospinal fibers. Eur J Neurosci 2006; 23: 1988–96.
90. FouadK, PedersenV, SchwabME, et al. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr Biol 2001; 11: 1766–70.
91. GhoshA, HaissF, SydekumE, et al. Rewiring of hindlimb corticospinal neurons after spinal cord injury. Nat Neurosci 2010; 13: 97–104.
92. GhoshA, SydekumE, HaissF, et al. Functional and anatomical reorganization of the sensory-motor cortex after incomplete spinal cord injury in adult rats. J Neurosci 2009; 29: 12210–9.
93. RosenzweigES, CourtineG, JindrichDL, et al. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci 2010; 13: 1505–10.
94. McKeonRJ, HökeA, SilverJ. Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Exp Neurol 1995; 136: 32–43.
95. AsherRA, MorgensternDA, ShearerMC, et al. Versican is up-regulated in CNS injury and is a product of oligodendrocyte lineage cells. J Neurosci 2002; 22: 2225–36.
96. BradburyEJ, MoonLD, PopatRJ, et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 2002; 416: 636–40.
97. YickLW, CheungPT, SoKF, et al. Axonal regeneration of Clarke’s neurons beyond the spinal cord injury scar after treatment with chondroitinase ABC. Exp Neurol 2003; 182: 160–8.
98. ShieldsLB, ZhangYP, BurkeDA, et al. Benefit of chondroitinase ABC on sensory axon regeneration in a laceration model of spinal cord injury in the rat. Surg Neurol 2008; 69: 568–77.
99. CaggianoAO, ZimberMP, GangulyA, et al. Chondroitinase ABCI improves locomotion and bladder function following contusion injury of the rat spinal cord. J Neurotrauma 2005; 22: 226–39.
100. TesterNJ, HowlandDR. Chondroitinase ABC improves basic and skilled locomotion in spinal cord injured cats. Exp Neurol 2008; 209: 483–96.
101. JeffersonSC, TesterNJ, HowlandDR. Chondroitinase ABC promotes recovery of adaptive limb movements and enhances axonal growth caudal to a spinal hemisection. J Neurosci 2011; 31: 5710–20.
102. BarrittAW, DaviesM, MarchandF, et al. Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury. J Neurosci 2006; 26: 10856–67.
103. Garcia-AliasG, LinR, AkrimiSF, et al. Therapeutic time window for the application of chondroitinase ABC after spinal cord injury. Exp Neurol 2008; 210: 331–8.
104. CaffertyWB, BradburyEJ, LidierthM, et al. Chondroitinase ABC-mediated plasticity of spinal sensory function. J Neurosci 2008; 28: 11998–2009.
105. GaltreyCM, AsherRA, NothiasF, et al. Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain 2007; 130: 926–39.
106. WieselTN, HubelDH. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol 1965; 28: 1029–40.
107. FagioliniM, PizzorussoT, BerardiN, et al. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res 1994; 34: 709–20.
108. PizzorussoT, MediniP, BerardiN, et al. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 2002; 298: 1248–51.
109. PizzorussoT, MediniP, LandiS, et al. Structural and functional recovery from early monocular deprivation in adult rats. PNAS 2006; 103: 8517–22.
110. TropeaD, CaleoM, MaffeiL. Synergistic effects of brain-derived neurotrophic factor and chondroitinase ABC on retinal fiber sprouting after denervation of the superior colliculus in adult rats. J Neurosci 2003; 23: 7034–44.
111. GogollaN, CaroniP, LüthiA, et al. Perineuronal nets protect fear memories from erasure. Science 2009; 325: 1258–61.
112. CorvettiL, RossiF. Degradation of chondroitin sulfate proteoglycan induces sprouting of intact purkinje axons in the cerebellum of the adult rat. J Neurosci 2005; 25: 7150–8.
113. FrischknechtR, HeineM, PerraisD, et al. Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 2009; 12: 897–904.
114. LovelyRG, GregorRJ, RoyRR, et al. Effects of training on the recovery of full-weight-bearing stepping in the adult spinal cat. Exp Neurol 1986; 92: 421–35.
115. IchiyamaRM, CourtineG, GerasimenkoYP, et al. Step training reinforces specific spinal locomotor circuitry in adult spinal rats. J Neurosci 2008; 28: 7370–5.
116. GrillnerS, WallénP. Central pattern generators for locomotion, with special reference to vertebrates. Annu Rev Neurosci 1985; 8: 233–61.
117. BrownstoneRM, WilsonJM. Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis. Brain Res Rev 2008; 57: 64–76.
118. LanderC, KindP, MaleskiM, et al. A family of activity-dependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. J Neurosci 1997; 17: 1928–39.
119. McRaePA, RoccoMM, KellyG, et al. Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci 2007; 27: 5405–13.
120. KalbRG, HockfieldS. Molecular evidence for early activity-dependent development of hamster motor neurons. J Neurosci 1988; 8: 2350–60.
121. SaleA, Maya VetencourtJF, MediniP, et al. Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat Neurosci 2007; 10: 679–81.
122. MiyataS, AkagiA, HayashiN, et al. Activity-dependent regulation of a chondroitin sulfate proteoglycan 6B4 phosphacan/RPTPbeta in the hypothalamic supraoptic nucleus. Brain Res 2004; 1017: 163–71.
123. GirgisJ, MerrettD, KirklandS, et al. Reaching training in rats with spinal cord injury promotes plasticity and task specific recovery. Brain 2007; 130: 2993–3003.
124. de LeonRD, HodgsonJA, RoyRR, et al. Full weight-bearing hindlimb standing following stand training in the adult spinal cat. J Neurophysiol 1998; 80: 83–91.
125. de LeonRD, HodgsonJA, RoyRR, et al. Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J Neurophysiol 1998; 79: 1329–40.
126. AllredRP, JonesTA. Maladaptive effects of learning with the less-affected forelimb after focal cortical infarcts in rats. Exp Neurol 2008; 210: 172–81.
127. WangD, IchiyamaRM, ZhaoR, et al. Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J Neurosci 2011; 31: 9332–44.
128. KrajacicA, GhoshM, PuentesR, et al. Advantages of delaying the onset of rehabilitative reaching training in rats with incomplete spinal cord injury. Eur J Neurosci 2009; 29: 641–51.
129. Karimi-AbdolrezaeeS, EftekharpourE, et al. Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J Neurosci 2010; 30: 1657–76.
130. TomVJ, Sandrow-FeinbergHR, MillerK, et al. Combining peripheral nerve grafts and chondroitinase promotes functional axonal regeneration in the chronically injured spinal cord. J Neurosci 2009; 29: 14881–90.