Animal models of post-ischemic forced use rehabilitation: Methods, considerations, and limitations

Experimental and Translational Stroke Medicine

Volumn 5, Issue 1, 2013, Pages

  Livingston Thomas, Jessica M ^a   Tasker, R Andrew ^a  

^a UNIVERSITY OF PRINCE EDWARD ISLAND   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIN 1;

CEREBROVASCULAR ACCIDENT; CONVALESCENCE; DEVASCULARIZATION; DISABILITY SEVERITY; DISEASE COURSE; FUNCTIONAL ASSESSMENT; FUNCTIONAL STATUS; HEMIPLEGIA; MIDDLE CEREBRAL ARTERY; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR ACTIVITY; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; SENSORIMOTOR FUNCTION; THROMBOSIS; TRANSLATIONAL RESEARCH; WALKING DIFFICULTY;

EID: 84875348134     PISSN: None     EISSN: 20407378     Source Type: Journal    
DOI: 10.1186/2040-7378-5-2     Document Type: Review

References (106)

1. Brodal A. Self-observations and neuro-anatomical considerations after a stroke. Brain 1973, 96:675-694. 10.1093/brain/96.4.675, 4773860.
2. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM, Carnethon MR, Dai S, De Simone G, Ford ES, Fox CS, Fullerton HJ, Gillespie C, Greenlund KJ, Hailpern SM, Heit JA, Ho PM, Howard VJ, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Makuc DM, Marcus GM, Marelli A, Matchar DB, McDermott MM, Meigs JB, Moy CS. Heart disease and stroke statistics--2011 update: a report from the American Heart Association. Circulation 2011, 123:e18-e209. et al, 10.1161/CIR.0b013e3182009701, 21160056.
3. Stroke statistics [http://www.heartandstroke.pe.ca/site/c.inKLKROwHqE/b.3646337/k.3514/Statistics.htm].
4. Burvill P, Johnson G, Jamrozik K, Anderson C, Stewart-Wynne E. Risk factors for post-stroke depression. Int J Geriatr Psychiatry 1997, 12:219-26. 10.1002/(SICI)1099-1166(199702)12:2<219::AID-GPS581>3.0.CO;2-E, 9097215.
5. Bousser MG. Stroke prevention: an update. Front Med 2012, 6:22-34. 10.1007/s11684-012-0178-6, 22460445.
6. Zhang ZG, Chopp M. Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol 2009, 8:491-500. 10.1016/S1474-4422(09)70061-4, 2727708, 19375666.
7. Madden K. Optimal timing of thrombolytic therapy in acute ischaemic stroke. CNS Drugs 2002, 16:213-218. 10.2165/00023210-200216040-00001, 11945105.
8. Stemer A, Lyden P. Evolution of the thrombolytic treatment window for acute ischemic stroke. Curr Neurol Neurosci Rep 2010, 10:29-33. 10.1007/s11910-009-0076-8, 2828551, 20425223.
9. STAIR Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 1999, 30:2752-2758. STAIR.
10. Nijland R, Kwakkel G, Bakers J, Van Wegen E. Constraint-induced movement therapy for the upper paretic limb in acute or sub-acute stroke: a systematic review. Int J Stroke 2011, 6:425-433. 10.1111/j.1747-4949.2011.00646.x, 21951408.
11. Taub E, Uswatte G, Mark VW, Morris DM. The learned nonuse phenomenon: implications for rehabilitation. Eura Medicophys 2006, 42:241-256.
12. Wittenberg GF, Chen R, Ishii K, Bushara KO, Eckloff S, Croarkin E, Taub E, Gerber LH, Hallett M, Cohen LG. Constraint-induced therapy in stroke: magnetic-stimulation motor maps and cerebral activation. Neurorehabil Neural Repair 2003, 17:48-57. 10.1177/0888439002250456, 12645445.
13. Sawaki L, Butler AJ, Xiaoyan L, Wassenaar PA, Mohammad YM, Blanton S, Sathian K, Nichols-Larsen DS, Wolf SL, Good DC, Wittenberg GF. Constraint-Induced Movement Therapy Results in Increased Motor Map Area in Subjects 3 to 9 Months After Stroke. Neurorehabil Neural Repair 2011, 22:505-513.
14. Morris D, Taub E, Mark V. Constraint-induced movement therapy: Characterizing the intervention protocol. Eura Medicophys 2006, 42:257-268.
15. Wolf SL, Thompson PA, Winstein CJ, Miller JP, Blanton SR, Nichols-Larsen DS, Morris DM, Uswatte G, Taub E, Light KE, Sawaki L. The EXCITE Stroke Trial: Comparing Early and Delayed Constraint-Induced Movement Therapy. Stroke 2011, 41:2309-2315.
16. Bonaiuti D, Rebasti L, Sioli P. The constraint induced movement therapy: a systematic review of randomised controlled trials on the adult stroke patients. Eura Medicophys 2007, 43:139-146.
17. Taub E, Uswatte G, King DK, Morris D, Crago JE, Chatterjee A. A placebo-controlled trial of constraint-induced movement therapy for upper extremity after stroke. Stroke 2006, 37:1045-1049. 10.1161/01.STR.0000206463.66461.97, 16514097.
18. Taub E, Uswatte G. Constraint-induced movement therapy: bridging from the primate laboratory to the stroke rehabilitation laboratory. J Rehabil Med 2003, 35:34-40.
19. Page SJ, Levine P, Sisto S, Bond Q, Johnston MV. Stroke patients' and therapists' opinions of constraint-induced movement therapy. Clin Rehabil 2002, 16:55-60. 10.1191/0269215502cr473oa, 11837526.
20. Page SJ, Levine P, Leonard AC. Modified constraint-induced therapy in acute stroke: a randomized controlled pilot study. Neurorehabil Neural Repair 2005, 19:27-32. 10.1177/1545968304272701, 15673841.
21. Sterr A, Elbert T, Berthold I, Kolbel S, Rockstroh B, Taub E. Longer versus shorter daily constraint-induced movement therapy of chronic hemiparesis: an exploratory study. Arch Phys Med Rehabil 2002, 83:1374-1377. 10.1053/apmr.2002.35108, 12370871.
22. Richards L, Gonzalez Rothi LJ, Davis S, Wu SS, Nadeau SE. Limited dose response to constraint-induced movement therapy in patients with chronic stroke. Clin Rehabil 2006, 20:1066-1074. 10.1177/0269215506071263, 17148518.
23. Sterr A, Saunders A. CI therapy distribution: theory, evidence and practice. NeuroRehabilitation 2006, 21:97-105.
24. Mark VW, Taub E. Constraint-induced movement therapy for chronic stroke hemiparesis and other disabilities. Restorative Neurol Neurosci 2004, 22:317-336.
25. Schabitz WR, Berger C, Kollmar R, Seitz M, Tanay E, Kiessling M, Schwab S, Sommer C. Effect of brain-derived neurotrophic factor treatment and forced arm use on functional motor recovery after small cortical ischemia. Stroke 2004, 35:992-997. 10.1161/01.STR.0000119754.85848.0D, 14988579.
26. Leasure JL, Schallert T. Consequences of forced disuse of the impaired forelimb after unilateral cortical injury. Behav Brain Res 2004, 150:83-91. 10.1016/S0166-4328(03)00254-7, 15033282.
27. DeBow SB, Davies ML, Clarke HL, Colbourne F. Constraint-induced movement therapy and rehabilitation exercises lessen motor deficits and volume of brain injury after striatal hemorrhagic stroke in rats. Stroke 2003, 34:1021-1026. 10.1161/01.STR.0000063374.89732.9F, 12649509.
28. Humm JL, Kozlowski DA, James DC, Gotts JE, Schallert T. Use-dependent exacerbation of brain damage occurs during an early post-lesion vulnerable period. Brain Res 1998, 783:286-292. 10.1016/S0006-8993(97)01356-5, 9507166.
29. Müller HD, Hanumanthiah KM, Diederich K, Schwab S, Schäbitz W-R, Sommer C. Brain-derived neurotrophic factor but not forced arm use improves long-term outcome after photothrombotic stroke and transiently upregulates binding densities of excitatory glutamate receptors in the rat brain. Stroke 2008, 39:1012-1021. 10.1161/STROKEAHA.107.495069, 18239176.
30. Bland ST, Schallert T, Strong R, Aronowski J, Grotta JC, Feeney DM. Early exclusive use of the affected forelimb after moderate transient focal ischemia in rats: functional and anatomic outcome. Stroke 2000, 31:1144-1152. 10.1161/01.STR.31.5.1144, 10797179.
31. Imai H, Konno K, Nakamura M, Shimizu T, Kubota C, Seki K, Honda F, Tomizawa S, Tanaka Y, Hata H, Saito N. A new model of focal cerebral ischemia in the miniature pig. Journal Neurosurg 2006, 104:123-132.
32. Watanabe O, Bremer AM, West CR. Experimental regional cerebral ischemia in the middle cerebral artery territory in primates. Part 1: Angio-anatomy and description of an experimental model with selective embolization of the internal carotid artery bifurcation. Stroke 1977, 8:61-70. 10.1161/01.STR.8.1.61, 402041.
33. Mhairi Macrae I. New models of focal cerebral ischaemia. Br J Clin Pharmacol 1992, 34:302-308. 10.1111/j.1365-2125.1992.tb05634.x, 1381409, 1457262.
34. Yamori Y, Horie R, Handa H, Sato M, Fukase M. Spontaneously Hypertensive Rats and Humans. Stroke 1976, 7:46-53. 10.1161/01.STR.7.1.46, 1258104.
35. Durukan A, Tatlisumak T. Acute ischemic stroke: overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia. Pharmacol Biochem Behav 2007, 87:179-197. 10.1016/j.pbb.2007.04.015, 17521716.
36. Tamura A, Graham DI, McCulloch J, Teasdale GM. Focal cerebral ischaemia in the rat: 1. Description of technique and early neuropathological consequences following middle cerebral artery occlusion. J Cerebral Blood Flow Metab 1981, 1:53-60.
37. Whishaw IQ, Suchowersky O, Davis L, Sarna J, Metz GA, Pellis SM. Impairment of pronation, supination, and body co-ordination in reach-to-grasp tasks in human Parkinson's disease (PD) reveals homology to deficits in animal models. Behav Brain Res 2002, 133:165-176. 10.1016/S0166-4328(01)00479-X, 12110450.
38. Walberer M, Stolz E, Muller C, Friedrich C, Rottger C, Blaes F, Kaps M, Fisher M, Bachmann G, Gerriets T. Experimental stroke: ischaemic lesion volume and oedema formation differ among rat strains (a comparison between Wistar and Sprague-Dawley rats using MRI). Lab Anim 2006, 40:1-8. 10.1258/002367706775404426, 16460584.
39. Sauter A, Rudin M. Strain-Dependent Occlusion Model Drug Effects of Stroke in Rat Middle Cerebral Artery. J Pharmacol Exp Ther 1995, 274:1008-1013.
40. Lindner MD, Gribkoff VK, Donlan NA, Jones TA. Long-lasting functional disabilities in middle-aged rats with small cerebral infarcts. J Neurosci 2003, 23:10913-10922.
41. Pan Y, Zhang H, Acharya AB, Patrick PH, Oliver D, Morley JE. Effect of testosterone on functional recovery in a castrate male rat stroke model. Brain Res 2005, 1043:195-204. 10.1016/j.brainres.2005.02.078, 15862533.
42. Ryan CL, Doucette TA, Gill DA, Langdon KD, Liu Y, Perry MA, Tasker RA. An improved post-operative care protocol allows detection of long-term functional deficits following MCAo surgery in rats. J Neurosci Methods 2006, 154:30-37. 10.1016/j.jneumeth.2005.11.009, 16423407.
43. Soleman S, Yip P, Leasure JL, Moon L. Sustained sensorimotor impairments after endothelin-1 induced focal cerebral ischemia (stroke) in aged rats. Exp Neurol 2010, 222:13-24. 10.1016/j.expneurol.2009.11.007, 2864515, 19913535.
44. Leasure JL, Grider M. The effect of mild post-stroke exercise on reactive neurogenesis and recovery of somatosensation in aged rats. Exp Neurol 2010, 226:58-67. 10.1016/j.expneurol.2010.08.003, 20696163.
45. Jones TA, Allred RP, Adkins DL, Hsu JE, O'Bryant A, Maldonado MA. Remodeling the brain with behavioral experience after stroke. Stroke 2009, 40:S136-8. 10.1161/STROKEAHA.108.533653, 2683888, 19064784.
46. Dobkin BH. Neurobiology of rehabilitation. Ann NY Acad Sci 2004, 1038:148-170. 10.1196/annals.1315.024, 15838110.
47. Wieloch T, Nikolich K. Mechanisms of neural plasticity following brain injury. Curr Opin Neurobiol 2006, 16:258-264. 10.1016/j.conb.2006.05.011, 16713245.
48. Boyko M, Zlotnik A, Gruenbaum BF, Gruenbaum SE, Ohayon S, Goldsmith T, Kotz R, Leibowitz A, Sheiner E, Shapira Y, Teichberg VI. An experimental model of focal ischemia using an internal carotid artery approach. J Neurosci Methods 2010, 193:246-253. 10.1016/j.jneumeth.2010.08.026, 20817031.
49. Belayev L, Alonso OF, Busto R, Zhao W, Ginsberg MD. Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model. Stroke 1996, 27:1616-1622. discussion 1623, 10.1161/01.STR.27.9.1616, 8784138.
50. Pena-Tapia PG, Diaz AH, Torres JL. Permanent endovascular occlusion of the middle cerebral artery in Wistar rats: a description of surgical approach through the internal carotid artery. Rev Neurol 2004, 39:1011-1016.
51. Lipsanen A, Jolkkonen J. Experimental approaches to study functional recovery following cerebral ischemia. Cell Mol Life Sciences 2011, 68:3007-3017.
52. Gerriets T, Stolz E, Walberer M, Müller C, Rottger C, Kluge A, Kaps M, Fisher M, Bachmann G. Complications and pitfalls in rat stroke models for middle cerebral artery occlusion: a comparison between the suture and the macrosphere model using magnetic resonance angiography. Stroke 2004, 35:2372-7. 10.1161/01.STR.0000142134.37512.a7, 15345802.
53. Trueman RC, Harrison DJ, Dwyer DM, Dunnett SB, Hoehn M, Farr TD. A Critical Re-Examination of the Intraluminal Filament MCAO Model: Impact of External Carotid Artery Transection. Transl Stroke Res 2011, 2:651-661.
54. Fuxe K, Kurosawa N, Cintra A, Hallstrom A, Goiny M, Rosen L, Agnati LF, Ungerstedt U. Involvement of local ischemia in endothelin-1 induced lesions of the neostriatum of the anaesthetized rat. Exp Brain Res 1992, 88:131-139. 10.1007/BF02259134, 1541348.
55. Adkins DL, Hsu JE, Jones TA. Motor cortical stimulation promotes synaptic plasticity and behavioral improvements following sensorimotor cortex lesions. Exp Neurol 2008, 212:14-28. 10.1016/j.expneurol.2008.01.031, 3018150, 18448100.
56. Windle V, Szymanska A, Granter-Button S, White C, Buist R, Peeling J, Corbett D. An analysis of four different methods of producing focal cerebral ischemia with endothelin-1 in the rat. Exp Neurol 2006, 201:324-334. 10.1016/j.expneurol.2006.04.012, 16740259.
57. Livingston-Thomas JM, Hume AW, Doucette TA, Tasker RA. A novel approach to induction and rehabilitation of deficits in forelimb function in a rat model of ischemic stroke. Acta Pharmacol Sin 2012, 1-9.
58. Sharkey J, Ritchie IM, Kelly PA. Perivascular microapplication of endothelin-1: a new model of focal cerebral ischaemia in the rat. J Cereb Blood Flow Metab 1993, 13:865-871. 10.1038/jcbfm.1993.108, 8360292.
59. Kleim JA, Boychuk JA, Adkins DL. Rat models of upper extremity impairment in stroke. ILAR J 2007, 48:374-384. 10.1093/ilar.48.4.374, 17712223.
60. Frost SB, Barbay S, Mumert ML, Stowe AM, Nudo RJ. An animal model of capsular infarct: endothelin-1 injections in the rat. Behav Brain Res 2006, 169:206-211. 10.1016/j.bbr.2006.01.014, 16497394.
61. Watson BD, Dietrich WD, Busto R, Wachtel MS, Ginsberg MD. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol 1985, 17:497-504. 10.1002/ana.410170513, 4004172.
62. Yao H, Sugimori H, Fukuda K, Takada J, Ooboshi H, Kitazono T, Ibayashi S, Iida M. Photothrombotic middle cerebral artery occlusion and reperfusion laser system in spontaneously hypertensive rats. Stroke 2003, 34:2716-21. 10.1161/01.STR.0000094730.38343.73, 14576380.
63. Yao H, Nabika T. Characterizing photothrombotic distal middle cerebral artery occlusion and YAG laser-induced reperfusion model in the Izumo strain of spontaneously hypertensive rats. Cell Mol Neurobiol 2011, 31:57-63. 10.1007/s10571-010-9553-5, 20703797.
64. Markgraf CG, Kraydieh S, Prado R, Watson BD, Dietrich WD, Ginsberg MD. Comparative histopathologic consequences of photothrombotic occlusion of the distal middle cerebral artery in Sprague-Dawley and Wistar rats. Stroke 1993, 24:283-286.
65. Shanina EV, Schallert T, Witte OW, Redecker C. Behavioral recovery from unilateral photothrombotic infarcts of the forelimb sensorimotor cortex in rats: role of the contralateral cortex. Neuroscience 2006, 139:1495-1506. 10.1016/j.neuroscience.2006.01.016, 16516395.
66. Carmichael ST. Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2005, 2:396-409. 10.1602/neurorx.2.3.396, 1144484, 16389304.
67. Metz GA, Whishaw IQ. Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore- and hindlimb stepping, placing, and co-ordination. J Neurosci Methods 2002, 115:169-179. 10.1016/S0165-0270(02)00012-2, 11992668.
68. Whishaw IQ. Loss of the innate cortical engram for action patterns used in skilled reaching and the development of behavioral compensation following motor cortex lesions in the rat. Neuropharmacology 2000, 39:788-805. 10.1016/S0028-3908(99)00259-2, 10699445.
69. Gonzalez CL, Kolb B. A comparison of different models of stroke on behaviour and brain morphology. Eur J Neurosci 2003, 18:1950-1962. 10.1046/j.1460-9568.2003.02928.x, 14622227.
70. Hossmann K-A. Cerebral ischemia: models, methods and outcomes. Neuropharmacology 2008, 55:257-270. 10.1016/j.neuropharm.2007.12.004, 18222496.
71. Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989, 20:84-91. 10.1161/01.STR.20.1.84, 2643202.
72. Fuxe K, Bjelke B, Andbjer B, Grahn H, Rimondini R, Agnati LF. Endothelin-1 induced lesions of the frontoparietal cortex of the rat. A possible model of focal cortical ischemia. NeuroReport 1997, 8:2623-2629. 10.1097/00001756-199707280-00040, 9261839.
73. Yanagita S, Amemiya S, Suzuki S, Kita I. Effects of spontaneous and forced running on activation of hypothalamic corticotropin-releasing hormone neurons in rats. Life Sci 2007, 80:356-363. 10.1016/j.lfs.2006.09.027, 17067638.
74. Ke Z, Yip SP, Li L, Zheng XX, Tong KY. The effects of voluntary, involuntary, and forced exercises on brain-derived neurotrophic factor and motor function recovery: a rat brain ischemia model. PLoS One 2011, 6:e16643. 10.1371/journal.pone.0016643, 3035657, 21347437.
75. Muller HD, Hanumanthiah KM, Diederich K, Schwab S, Schabitz WR, Sommer C. Brain-derived neurotrophic factor but not forced arm use improves long-term outcome after photothrombotic stroke and transiently upregulates binding densities of excitatory glutamate receptors in the rat brain. Stroke 2008, 39:1012-1021. 10.1161/STROKEAHA.107.495069, 18239176.
76. Ploughman M, Windle V, MacLellan CL, White N, Dore JJ, Corbett D. Brain-derived neurotrophic factor contributes to recovery of skilled reaching after focal ischemia in rats. Stroke 2009, 40:1490-1495. 10.1161/STROKEAHA.108.531806, 19164786.
77. Maldonado MA, Allred RP, Felthauser EL, Jones TA. Motor skill training, but not voluntary exercise, improves skilled reaching after unilateral ischemic lesions of the sensorimotor cortex in rats. Neurorehabil Neural Repair 2008, 22:250-261. 10.1177/1545968307308551, 2586983, 18073324.
78. Auriat AM, Grams JD, Yan RH, Colbourne F. Forced exercise does not improve recovery after hemorrhagic stroke in rats. Brain Res 2006, 1109:183-191. 10.1016/j.brainres.2006.06.035, 16854389.
79. Yang YR, Wang RY, Wang PS. Early and late treadmill training after focal brain ischemia in rats. Neurosci Lett 2003, 339:91-94. 10.1016/S0304-3940(03)00010-7, 12614902.
80. Kim MW, Bang MS, Han TR, Ko YJ, Yoon BW, Kim JH, Kang LM, Lee KM, Kim MH. Exercise increased BDNF and trkB in the contralateral hemisphere of the ischemic rat brain. Brain Res 2005, 1052:16-21. 10.1016/j.brainres.2005.05.070, 16054599.
81. Marin R, Williams A, Hale S, Burge B, Mense M, Bauman R, Tortella F. The effect of voluntary exercise exposure on histological and neurobehavioral outcomes after ischemic brain injury in the rat. Physiol Behav 2003, 80:167-175. 10.1016/j.physbeh.2003.06.001, 14637213.
82. Biernaskie J, Corbett D. Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci 2001, 21:5272-5280.
83. Auriat AM, Wowk S, Colbourne F. Rehabilitation after intracerebral hemorrhage in rats improves recovery with enhanced dendritic complexity but no effect on cell proliferation. Behav Brain Res 2010, 214:42-47. 10.1016/j.bbr.2010.04.025, 20417236.
84. Auriat AM, Colbourne F. Delayed rehabilitation lessens brain injury and improves recovery after intracerebral hemorrhage in rats. Brain Res 2009, 1251:262-268.
85. MacLellan CL, Keough MB, Granter-Button S, Chernenko GA, Butt S, Corbett D. A critical threshold of rehabilitation involving brain-derived neurotrophic factor is required for poststroke recovery. Neurorehabil Neural Repair 2011, 25:740-748. 10.1177/1545968311407517, 21705652.
86. Biernaskie J, Chernenko G, Corbett D. Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. J Neurosci 2004, 24:1245-1254. 10.1523/JNEUROSCI.3834-03.2004, 14762143.
87. Ploughman M, Granter-Button S, Chernenko G, Attwood Z, Tucker BA, Mearow KM, Corbett D. Exercise intensity influences the temporal profile of growth factors involved in neuronal plasticity following focal ischemia. Brain Res 2007, 1150:207-216.
88. Hebb D. The Effects of Early Experience on Problem-Solving at Maturity. Am Psychol 1947, 2:306-307.
89. Janssen H, Bernhardt J, Collier JM, Sena ES, McElduff P, Attia J, Pollack M, Howells DW, Nilsson M, Calford MB, Spratt NJ. An enriched environment improves sensorimotor function post-ischemic stroke. Neurorehabil Neural Repair 2010, 24:802-813. 10.1177/1545968310372092, 20834046.
90. Fang PC, Barbay S, Plautz EJ, Hoover E, Strittmatter SM, Nudo RJ. Combination of NEP 1-40 treatment and motor training enhances behavioral recovery after a focal cortical infarct in rats. Stroke 2010, 41:544-549. 10.1161/STROKEAHA.109.572073, 2853474, 20075346.
91. Maclellan CL, Grams J, Adams K, Colbourne F. Combined use of a cytoprotectant and rehabilitation therapy after severe intracerebral hemorrhage in rats. Brain Res 2005, 1063:40-47. 10.1016/j.brainres.2005.09.027, 16269139.
92. DeBow SB, McKenna JE, Kolb B, Colbourne F. Immediate constraint-induced movement therapy causes local hyperthermia that exacerbates cerebral cortical injury in rats. Can J Physiol Pharmacol 2004, 82:231-237. 10.1139/y04-013, 15181461.
93. Chopp M, Li Y, Zhang J. Plasticity and remodeling of brain. J Neurol Sci 2008, 265:97-101. 10.1016/j.jns.2007.06.013, 17610903.
94. Carmichael ST, 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. 10.1016/j.expneurol.2005.01.004, 15869933.
95. Iadecola C, Anrather J. The immunology of stroke: from mechanisms to translation. Nat Med 2011, 17:796-808. 10.1038/nm.2399, 3137275, 21738161.
96. Madinier A, Bertrand N, Mossiat C, Prigent-Tessier A, Beley A, Marie C, Garnier P. Microglial involvement in neuroplastic changes following focal brain ischemia in rats. PLoS One 2009, 4:e8101. 10.1371/journal.pone.0008101, 2779656, 19956568.
97. Schaar KL, Brenneman MM, Savitz SI. Functional assessments in the rodent stroke model. Exp Trans Stroke Med 2010, 2:13.
98. Hicks AU, Lappalainen RS, Narkilahti S, Suuronen R, Corbett D, Sivenius J, Hovatta O, Jolkkonen J. Transplantation of human embryonic stem cell-derived neural precursor cells and enriched environment after cortical stroke in rats: cell survival and functional recovery. Eur J Neurosci 2009, 29:562-574. 10.1111/j.1460-9568.2008.06599.x, 19175403.
99. Hicks AU, MacLellan CL, Chernenko GA, Corbett D. Long-term assessment of enriched housing and subventricular zone derived cell transplantation after focal ischemia in rats. Brain Res 2008, 1231:103-112.
100. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39:777-787. 10.1016/S0028-3908(00)00005-8, 10699444.
101. Montoya CP, Campbell-Hope LJ, Pemberton KD, Dunnett SB. The " staircase test" : a measure of independent forelimb reaching and grasping abilities in rats. J Neurosci Methods 1991, 36:219-228. 10.1016/0165-0270(91)90048-5, 2062117.
102. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 1986, 17:472-476. 10.1161/01.STR.17.3.472, 3715945.
103. De Ryck M, Van Reempts J, Borgers M, Wauquier A, Janssen PA. Photochemical stroke model: flunarizine prevents sensorimotor deficits after neocortical infarcts in rats. Stroke 1989, 20:1383-1390. 10.1161/01.STR.20.10.1383, 2799870.
104. Huang H, Chang C, Lee T, Chang Y, Ryu S, Chang T, Huang K, Liu C, Chang H. Differential trajectory of functional recovery and determinants for first time stroke survivors by using a LCFA approach: a hosiptal based analysis over a 1-year period. Eur J Phys Rehabil Med 2012, 48:1-11.
105. Huang H-C, Chung K-C, Lai D-C, Sung S-F. The impact of timing and dose of rehabilitation delivery on functional recovery of stroke patients. J Chin Med Assoc 2009, 72:257-264. 10.1016/S1726-4901(09)70066-8, 19467949.
106. Duncan PW, Goldstein LB, Matchar D, Divine GW, Feussner J. Measurement of motor recovery after stroke. Outcome assessment and sample size requirements. Stroke 1992, 23:1084-1089. 10.1161/01.STR.23.8.1084, 1636182.