Curiosity and cure: Translational research strategies for neural repair-mediated rehabilitation

Developmental Neurobiology

Volumn 67, Issue 9, 2007, Pages 1133-1147

  Dobkin, Bruce H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Animal models; Neural repair; Rehabilitation; Spinal cord injury; Stroke

Indexed keywords

ADAPTATION; BEHAVIOR; CELL CULTURE; CELL PROLIFERATION; CELL TRANSPLANTATION; DISABLED PERSON; GENE ACTIVATION; HUMAN; INJURY SEVERITY; LEARNING; MEDICAL ETHICS; MEDICAL RESEARCH; NERVE FIBER REGENERATION; NERVE REGENERATION; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; REHABILITATION CARE; REMYELINIZATION; REVIEW; SPINAL CORD INJURY; STROKE; TRANSGENIC MOUSE;

ANIMALS; BRAIN DISEASES; CLINICAL TRIALS; DISEASE MODELS, ANIMAL; HUMANS; NERVE REGENERATION; SPINAL CORD DISEASES;

EID: 34547730638     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20514     Document Type: Review

References (94)

1. Albers GW, Amarenco P, Easton JD, Sacco RL, Teal P. 2004. Antithrombotic and thrombolytic therapy for ischemic stroke: The Seventh ACCP Conference on antithrombotic and thrombolytic therapy. Chest 126:483S-512S.
2. Anderson D, Beattie M, Blesch A, Bresnahan J, Bunge M, Dietrich D, Dietz V, et al. 2005. Recommended guidelines for studies of human subjects with spinal cord injury. Spinal Cord 43:453-458.
3. Bang O, Lee J, Lee P, Lee G. 2005. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol 57:874-882.
4. Barbeau H, Rossignol S. 1987. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 412:84-95.
5. Benowitz LI, Yin Y. 2007. Combinatorial treatments for promoting axon regeneration in the CNS: Strategies for overcoming inhibitory signals and activating neurons' intrinsic growth state. Dev Neurobiol 67:1148-1165.
6. Bilgen M. 2005. A new device for experimental modeling of central nervous system injuries. Neurorehabil Neural Repair 19:219-226.
7. Bracken M, Shepard M, Holford T, Leo-Summers L, Aldrich E, Fazi M, Fehlings M, et al. 1998. Results of the third acute spinal cord injury randomized controlled trial. J Neurosurg 89:699-706.
8. Bruce-Keller A, Umberger G, McFall R, Mattson M. 1999. Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Ann Neurol 45:8-15.
9. Bury S, Jones T. 2002. Unilateral sensorimotor cortex lesions in adult rats facilitate motor skill learning with the "unaffected" forelimb and training-induced dendritic structural plasticity in the motor cortex. J Neurosci 22:8597-8606.
10. Carey L, Abbott D, Egan G, O'Keefe G, Jackson G, Bernhardt J, Donnan G. 2006. Evolution of brain activation with good and poor motor recovery after stroke. Neurorehabil Neural Repair 20:42-48.
11. Carmichael S. 2003. Gene expression changes after focal stroke, traumatic brain and spinal cord injuries. Curr Opin Neurol 16:699-704.
12. Carmichael S. 2006. Cellular and molecular mechanisms of neural repair after stroke: Making waves. Ann Neurol 59:735-742.
13. Carmichael ST, Chesselet MF. 2002. Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. J Neurosci 22:6062-6070.
14. Chen P, Goldberg D, Kolb B, Lanser M, Benowitz L. 2002. Inosine induces axonal rewiring and improves behavioral outcome after stroke. Proc Natl Acad Sci 99: 9031-9036.
15. Conner JM, Chiba AA, Tuszynski MH. 2005. The basal forebrain cholinergic system is essential for cortical plasticity and functional recovery following brain injury. Neuron 46:173-179.
16. Dancause N, Barbay S, Frost SB, Plautz EJ, Chen D, Zoubina EV, Stowe AM, et al. 2005. Extensive cortical rewiring after brain injury. J Neurosci 25:10167-10179.
17. de Leon R, Hodgson J, Roy R, Edgerton V. 1998. Locomotor capacity attributable to step training versus spontaneous recovery after spinalization in adult cats. J Neurophysiol 79:1329-1340.
18. D'Hooge R, Deyn P. 2001. Applications of the Morris water maze in the study of learning and memory. Brain Res Rev 36:60-90.
19. Dietz V, Muller R, Colombo G. 2002. Locomotor activity in spinal man: Significance of afferent input from joint and load receptors. Brain 125:2626-2634.
20. Dimou L, Schnell L, Montani L, Duncan C, Simonen M, Schneider R, Gullo M, et al. 2006. Nogo-A-deficient mice strain-dependent differences in axonal regeneration. J Neurosci 26:5591-5603.
21. Dobkin B. 2003. The Clinical Science of Neurologic Rehabilitation. New York: Oxford University Press.
22. Dobkin B. 2004a. Strategies for stroke rehabilitation. Lancet Neurol 3:528-536.
23. Dobkin B. 2004b. The neurobiology of rehabilitation. Ann NY Acad Sci 1038:148-170.
24. Dobkin B. 2005a. Rehabilitation after stroke. New Engl J Med 352:1677-1684.
25. Dobkin B. 2007. Behavioral, temporal, and spatial targets for cellular transplants as adjuncts to rehabilitation for stroke. Stroke 38(2 Suppl):832-839.
26. Dobkin B, Barbeau H, Deforge D, Ditunno J, Elashoff R, Apple D, Basso M, et al. and SCILT Group. 2007. The evolution of walking-related outcomes over the first 12 weeks of rehabilitation for incomplete traumatic spinal cord injury: The SCILT multi-center randomized trial. Neurorehabil Neural Repair 21:23-35.
27. Dobkin B, Firestine A, West M, Saremi K, Woods R. 2004. Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation. Neuroimage 23:370-381.
28. Dobkin B, Havton L. 2004. Basic advances and new avenues in therapy of spinal cord injury. Annu Rev Med 55:255-282.
29. Dobkin BH. 2005b. Rehabilitation and functional neuroimaging dose-response trajectories for clinical trials. Neurorehabil Neural Repair 19:276-282.
30. Dobkin BH, Apple D, Barbeau H, Basso M, Behrman A, Deforge D, Ditunno J, et al. 2006a. Weight-supported treadmill vs over-ground training for walking after acute imcomplete SCI. Neurology 66:484-493.
31. Dobkin BH, Curt A, Guest J. 2006b. Cellular transplants in China: Observational study from the largest human experiment in chronic spinal cord injury. Neurorehabil Neural Repair 20:5-13.
32. Dong Y, Dobkin BH, Cen SY, Wu AD, Winstein CJ. 2006. Motor cortex activation during treatment may predict therapeutic gains in paretic hand function after stroke. Stroke 37:1552-1555.
33. Enserink M. 2006. Selling the stem cell dream. Science 313:160-163.
34. Feron F, Perry C, Cochrane J, Licina P, Nowitzke A, Urquhart S, Geraghty T, et al. 2005. Autologous olfactory ensheathing cell transplantation in human spinal cord injury. Brain 128:2951-2960.
35. Geisler F, Coleman W, Grieco G, Poonian D, Group SS. 2001. Measurements and recovery patterns in a multicenter study of acute spinal cord injury. Spine 26:S68-S86.
36. Gharbawie OA, Auer RN, Whishaw IQ. 2006. Subcortical middle cerebral artery ischemia abolishes the digit flexion and closing used for grasping in rat skilled reaching. Neuroscience 137:1107-1118.
37. Gonzalez C, Kolb B, Whishaw I. 2000. A cautionary note regarding drug and brain lesion studies that use swimming pool tasks. Behav Brain Res 112:43-52.
38. Green A, Odergren T, Ashwood T. 2003. Animal models of stroke: Do they have value for discovering neuroprotective agents? Trends Pharm Sci 24:402-408.
39. Guest J, Herrera L, Qian T. 2006. Rapid recovery of segmental neurological function in a tetraplegic patient following transplantation of fetal olfactory bulb-derived cells. Spinal Cord 44:135-142.
40. Guest J, Hiester E, Bunge R. 2005. Demyelination and Schwann cell responses adjacent to injury epicanter cavities following chronic human spinal cord injury. Exp Neurol 192:384-393.
41. Hagg T, Oudega M. 2006. Degenerative and spontaneous regenerative processes after spinal cord injury. J Neurotrauma 23:264-280.
42. Himes B, Neuhuber B, Coleman C, Kushner R, Swanger S, Kopen G, Wagner J, et al. 2006. Recovery of function following grafting of human bone marrow-derived stromal cells into the injured spinal cord. Neurorehabil Neural Repair 20:278-296.
43. Hoang T, Nieto J, Dobkin B, Tillakaratne N, Havton L. 2006. Acute implantation of an avulsed lumbosacral ventral root into the rat conus medullaris promotes neuroprotection and graft re innervation by autonomic and motor neurons. Neuroscience 138:1149-1160.
44. Ibrahim A, Li Y, Li D, Raisman G, El Masry WS. 2006. Olfactory ensheathing cells: Ripples of an incoming tide? Lancet Neurol 5:453-457.
45. Ivanenko YP, Cappellini G, Dominici N, Poppele RE, Lacquaniti F. 2005. Coordination of locomotion with voluntary movements in humans. J Neurosci 25:7238-7253.
46. Johansson B, Belichenko P. 2002. Neuronal plasticity and dendritic spines: Effect of environmental enrichment on intact and postischemic rat brain. J Cereb Blood Flow Metab 22:89-96.
47. Kakulas B. 1999. A review of the neuropathology of human spinal cord injury with emphasis on special features. J Spinal Cord Med 22:119-124.
48. Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O. 2005. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25:4694-4705.
49. Kondziolka D, Steinberg G, Wechsler L, Meltzer C, Elder E, Gebel J, Zafonte R, et al. 2005. Neurotransplantation for patients with subcortical motor stroke: A Phase 2 randomized trial. J Neurosurg 103:38-45.
50. Koski L, Mernar T, Dobkin B. 2004. Immediate and long-term changes in corticomotor output response to rehabilitation: Correlation with functional improvements in chronic stroke. Neurorehabil Neural Repair 18:230-249.
51. Kwakkel G, van Peppen R, Wagenaar R, Wood Dauphinee S, Richards C, Ashburn A, Miller K, et al. 2004. Effects of augmented exercise therapy time after stroke: A meta-analysis. Stroke 35:2529-2539.
52. Kwon B, Liu J, Messerer C, Kobayashi N, McGraw J, Oschipok L, Tetzlaff W. 2002. Survival and regeneration of rubrospinal neurons 1 year after spinal cord injury. Proc Natl Acad Sci USA 99:3246-3251.
53. Lacroix S, Havton LA, McKay H, Yang H, Brant A, Roberts J, Tuszynski MH. 2004. Bilateral corticospinal projections arise from each motor cortex in the macaque monkey: A quantitative study. J Comp Neurol 473:147-161.
54. Lees KR, Zivin JA, Ashwood T, Davalos A, Davis SM, Diener HC, Grotta J, et al. 2006. NXY-059 for acute ischemic stroke. N Engl J Med 354:588-600.
55. Lemon RN, Griffiths J. 2005. Comparing the function of the corticospinal system in different species: Organizational differences for motor specialization? Muscle Nerve 32:261-279.
56. Li S, Zheng J, Carmichael ST. 2005. Increased oxidative protein and DNA damage but decreased stress response in the aged brain following experimental stroke. Neurobiol Dis 18:432-440.
57. Lima C, Pratas-Vital J, Escada P, Hasse-Ferreira A, Capucho C, Peduzzi J. 2006. Olfactory mucosa autografts in human spinal cord injury: A pilot clinical study. J Spinal Cord Med 29:191-203.
58. Logan A, Ahmed Z, Baird A, Gonzalez AM, Berry M. 2006. Neurotrophic factor synergy is required for neuronal survival and disinhibited axon regeneration after CNS injury. Brain 129:490-502.
59. Lotze M, Grodd W, Rodden F, Gut E, Schonle P, Kardatzaki B, Cohen L. 2006. Neuroimaging patterns associated with motor control in traumatic brain injury. Neurorehabil Neural Repair 20:14-23.
60. Lu P, Yang H, Culbertson M, Graham M, Roskams A, Tuszynski M. 2006. Olfactory ensheathing cells do not exhibit unique migratory or axonal growth-promoting properties after spinal cord injury. J Neurosci 26:11120-11130.
61. Markus T, Tsai S-Y, Bollnow M, Farrer R, O'Brien T, Schwab M, Kartje G. 2005. Recovery and brain reorganization after stroke in adult and aged rats. Ann Neurol 58:950-953.
62. Mazevet D, Meunier S, Pradat-Diehl P, Marchand-Pauvert V, Pierrot-Deseilligny E. 2003. Changes in propriospinally mediated excitation of upper limb motoneurons in stroke patients. Brain 126:988-1000.
63. Mills C, Hains B, Johnson K, Hulsebosch C. 2001. Strain and model differences in behavioral outcomes after spinal cord injury in rat. J Neurotrauma 18:743-756.
64. Moseley A, Stark A, Cameron I, Pollack A. 2005. Treadmill training and body weight support for walking after stroke. Cochrane Database Syst Rev 4: CD002840. The Cochrane Library, Issue No. 4.
65. Moviglia G, Vina RF, Brizuela J, Saslavsky J, Vrsalovic F, Varela G, Bastois F, et al. 2006. Combined protocol of cell therapy for chronic spinal cord injury. Report of the electrical and functional recovery of two patients. Cytotherapy 8:202-209.
66. Narayan RK, Michel ME, Ansell B, Baethmann A, Biegon A, Bracken MB, Bullock MR, et al. 2002. Clinical trials in head injury. J Neurotrauma 19:503-557.
67. Nichols CM, Myckatyn TM, Rickman SR, Fox IK, Hadlock T, Mackinnon SE. 2005. Choosing the correct functional assay: A comprehensive assessment of functional tests in the rat. Behav Brain Res 163:143-158.
68. Nothias J-M, Mitsui T, Shumsky J, Fischer I, Antonacci M, Murray M. 2005. Combined effects of neurotrophin secreting transplants, exercise, and serotonergic drug challenge improve function in spinal rats. Neurorehabil Neural Repair 19:296-312.
69. Oka S, Honmou O, Akiyama Y, Sasaki M, Houkin K, Hashi K, Kocsis JD. 2004. Autologous transplantation of expanded neural precursor cells into the demyelinated monkey spinal cord. Brain Res 1030:94-102.
70. Piccini P, Pavese N, Hagell P, Reimer J, Bjorklund A, Oertel WH, Quinn NP, et al. 2005. Factors affecting the clinical outcome after neural transplantation in Parkinson's disease. Brain 128:2977-2986.
71. Ploughman M, Granter-Button S, Chernenko G, Tucker B, Mearow K, Corbett D. 2005. Endurance exercise regimens induce differential effects on brain-derived neurotrophic factor, synapsin-1, and insulin growth factor 1 after focal ischemia. Neurosci 136:991-1001.
72. Ralston D, Ralston H. 1985. The terminations of corticospinal tract axons in the macaque monkey. J Comp Neurol 242:325-337.
73. Ramos J. 2002. Training method dramatically affects the acquisition of a place response in rats with neurotoxic lesions of the hippocampus. Neurobiol Learn Mem 77:109-118.
74. Steeves J, Lammertse D, Curt A, Fawcett J, Tuszynski M, Bartlett P, Blight A, et al. 2007. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel. Spinal Cord 45:206-221.
75. Steinmetz M, Horn K, Tom V, Miller J, Busch S, Nair D, Silver D, et al. 2005. Chronic enhancement of the intrinsic growth capacity of sensory neurons combined with the degradation of inhibitory proteoglycans allows functional regeneration of sensory axons through the dorsal root entry zone in the mammalian spinal cord. J Neurosci 25:8066-8076.
76. Steward O, Schauwecker P, Guth L, Zhang Z, Fujiki M, Inman D, Wrathall J, et al. 1999. Genetic approaches to neurotrauma research: Opportunities and potential pitfalls of murine models. Exp Neurol 157:19-42.
77. Strangman G, Heindel W, Anderson J, Sutton J. 2005. Learning motor sequences with and without knowledge of governing rules. Neurorehabil Neural Repair 19:93-114.
78. Stroke Roundtable. 1999. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 30:2752-2758.
79. Tuszynski MH. 2007. Nerve growth factor gene delivery: Animal models to clinical trials. Dev Neurobiol 67: 1204-1215.
80. Tuszynski MH, Grill R, Jones LL, McKay HM, Blesch A. 2002. Spontaneous and augmented growth of axons in the primate spinal cord: Effects of local injury and nerve growth factor-secreting cell grafts. J Comp Neurol 449: 88-101.
81. Tuszynski M, Thai L, Pay M, Salmon D, Bakay R, Patel P, Blesch A, et al. 2005. A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat Med 11:551-555.
82. Van Dam D, Lenders G, De Deyn PP. 2006. Effect of Morris water maze diameter on visual-spatial learning in different mouse strains. Neurobiol Learn Mem 85:164-172.
83. Van der Harst J, Baars A-M, Spruit B. 2003. Standard housed rats are more sensitive to rewards than enriched housed rats as reflected by their anticipatory behavior. Behav Brain Res 142:151-156.
84. Van Praag H, Kempermann G, Gage F. 2000. Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191-198.
85. Vaynman S, Gomez-Pinilla F. 2005. License to run: Exercise impacts functional plasticity in the intact and injured CNS by using neurotrophins. Neurorehabil Neural Repair 19:283-295.
86. Wang W, van Niekerk E, Willis DE, Twiss JL. 2007. RNA transport and localized protein synthesis in neurological disorders and neural repair. Dev Neurobiol 67:1166-1182.
87. Webb A, Gowribai K, Muir G. 2003. Fischer rats have different morphology, sensorimotor and locomotor capabilities compared to Lewis, Long-Evans, Sprague-Dawley and Wistar rats. Behav Brain Res 144:143-156.
88. Webb AA, Muir GD. 2005. Sensorimotor behaviour following incomplete cervical spinal cord injury in the rat. Behav Brain Res 165:147-159.
89. Whishaw I, Kolb B. 2004. The Behavior of the Laboratory Rat: A Handbook with Tests. New York: Oxford University Press.
90. Wolpaw J, Tennissen A. 2001. Activity-dependent spinal cord plasticity in health and disease. Ann Rev Neurosci 24:807-843.
91. Wurbel H. 2001. Ideal homes? Housing effects on rodent brain and behavior. Trends Neurosci 24:207-211.
92. Yang H, Lu P, McKay H, Bernot T, Keirstead H, Steward O, Gage F, et al. 2006. Endogenous neurogenesis replaces oligodendrocytes and astrocytes after primate spinal cord injury. J Neuroscience 26:2157-2166.
93. Zhang G, Jin L-Q, Sul J-Y, Haydon P, Selzer M. 2005. Live imaging of regenerating lamprey spinal axons. Neurorehabil Neural Repair 19:46-57.
94. Ziemann U, Meintzschel F, Korchounov A, Ilic TV. 2006. Pharmacological modulation of plasticity in the human motor cortex. Neurorehabil Neural Repair 20:243-251.