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Published in: Experimental & Translational Stroke Medicine 1/2013

Open Access 01-12-2013 | Review

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

Authors: Jessica M Livingston-Thomas, R Andrew Tasker

Published in: Experimental & Translational Stroke Medicine | Issue 1/2013

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Abstract

Many survivors of stroke experience arm impairments, which can severely impact their quality of life. Forcing use of the impaired arm appears to improve functional recovery in post-stroke hemiplegic patients, however the mechanisms underlying improved recovery remain unclear. Animal models of post-stroke rehabilitation could prove critical to investigating such mechanisms, however modeling forced use in animals has proven challenging. Potential problems associated with reported experimental models include variability between stroke methods, rehabilitation paradigms, and reported outcome measures. Herein, we provide an overview of commonly used stroke models, including advantages and disadvantages of each with respect to studying rehabilitation. We then review various forced use rehabilitation paradigms, and highlight potential difficulties and translational problems. Lastly, we discuss the variety of functional outcome measures described by experimental researchers. To conclude, we outline ongoing challenges faced by researchers, and the importance of translational communication. Many stroke patients rely critically on rehabilitation of post-stroke impairments, and continued effort toward progression of rehabilitative techniques is warranted to ensure best possible treatment of the devastating effects of stroke.
Appendix
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Literature
1.
go back to reference Brodal A: Self-observations and neuro-anatomical considerations after a stroke. Brain 1973, 96: 675–694. 10.1093/brain/96.4.675PubMed Brodal A: Self-observations and neuro-anatomical considerations after a stroke. Brain 1973, 96: 675–694. 10.1093/brain/96.4.675PubMed
2.
go back to reference 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.0b013e3182009701PubMedCentralPubMed 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.0b013e3182009701PubMedCentralPubMed
4.
go back to reference 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-EPubMed 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-EPubMed
5.
go back to reference Bousser MG: Stroke prevention: an update. Front Med 2012, 6: 22–34. 10.1007/s11684-012-0178-6PubMed Bousser MG: Stroke prevention: an update. Front Med 2012, 6: 22–34. 10.1007/s11684-012-0178-6PubMed
6.
go back to reference 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)70061-4PubMedCentralPubMed 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)70061-4PubMedCentralPubMed
7.
go back to reference Madden K: Optimal timing of thrombolytic therapy in acute ischaemic stroke. CNS Drugs 2002, 16: 213–218. 10.2165/00023210-200216040-00001PubMed Madden K: Optimal timing of thrombolytic therapy in acute ischaemic stroke. CNS Drugs 2002, 16: 213–218. 10.2165/00023210-200216040-00001PubMed
8.
go back to reference Stemer A, Lyden P: Evolution of the thrombolytic treatment window for acute ischemic stroke. Curr Neurol Neurosci Rep 2010, 10: 29–33. 10.1007/s11910-009-0076-8PubMedCentralPubMed Stemer A, Lyden P: Evolution of the thrombolytic treatment window for acute ischemic stroke. Curr Neurol Neurosci Rep 2010, 10: 29–33. 10.1007/s11910-009-0076-8PubMedCentralPubMed
9.
go back to reference STAIR: Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 1999, 30: 2752–2758. STAIR: Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 1999, 30: 2752–2758.
10.
go back to reference 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.xPubMed 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.xPubMed
11.
go back to reference Taub E, Uswatte G, Mark VW, Morris DM: The learned nonuse phenomenon: implications for rehabilitation. Eura Medicophys 2006, 42: 241–256.PubMed Taub E, Uswatte G, Mark VW, Morris DM: The learned nonuse phenomenon: implications for rehabilitation. Eura Medicophys 2006, 42: 241–256.PubMed
12.
go back to reference 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. 10.1177/0888439002250456PubMed 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. 10.1177/0888439002250456PubMed
13.
go back to reference 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. 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.
go back to reference Morris D, Taub E, Mark V: Constraint-induced movement therapy: Characterizing the intervention protocol. Eura Medicophys 2006, 42: 257–268.PubMed Morris D, Taub E, Mark V: Constraint-induced movement therapy: Characterizing the intervention protocol. Eura Medicophys 2006, 42: 257–268.PubMed
15.
go back to reference 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. 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.
go back to reference 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.PubMed 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.PubMed
17.
go back to reference 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.0000206463.66461.97PubMed 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.0000206463.66461.97PubMed
18.
go back to reference 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. 10.1080/16501960310010124 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. 10.1080/16501960310010124
19.
go back to reference 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. 10.1191/0269215502cr473oaPubMed 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. 10.1191/0269215502cr473oaPubMed
20.
go back to reference 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. 10.1177/1545968304272701PubMed 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. 10.1177/1545968304272701PubMed
21.
go back to reference 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.2002.35108PubMed 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.2002.35108PubMed
22.
go back to reference 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. 10.1177/0269215506071263PubMed 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. 10.1177/0269215506071263PubMed
23.
go back to reference Sterr A, Saunders A: CI therapy distribution: theory, evidence and practice. NeuroRehabilitation 2006, 21: 97–105.PubMed Sterr A, Saunders A: CI therapy distribution: theory, evidence and practice. NeuroRehabilitation 2006, 21: 97–105.PubMed
24.
go back to reference Mark VW, Taub E: Constraint-induced movement therapy for chronic stroke hemiparesis and other disabilities. Restorative Neurol Neurosci 2004, 22: 317–336. Mark VW, Taub E: Constraint-induced movement therapy for chronic stroke hemiparesis and other disabilities. Restorative Neurol Neurosci 2004, 22: 317–336.
25.
go back to reference 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.0000119754.85848.0DPubMed 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.0000119754.85848.0DPubMed
26.
go back to reference 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)00254-7PubMed 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)00254-7PubMed
27.
go back to reference 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.0000063374.89732.9FPubMed 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.0000063374.89732.9FPubMed
28.
go back to reference 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)01356-5PubMed 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)01356-5PubMed
29.
go back to reference 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.107.495069PubMed 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.107.495069PubMed
30.
go back to reference 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.31.5.1144PubMed 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.31.5.1144PubMed
31.
go back to reference 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. 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.
go back to reference 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.8.1.61PubMed 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.8.1.61PubMed
33.
go back to reference Mhairi Macrae I: New models of focal cerebral ischaemia. Br J Clin Pharmacol 1992, 34: 302–308. 10.1111/j.1365-2125.1992.tb05634.xPubMedCentralPubMed Mhairi Macrae I: New models of focal cerebral ischaemia. Br J Clin Pharmacol 1992, 34: 302–308. 10.1111/j.1365-2125.1992.tb05634.xPubMedCentralPubMed
34.
go back to reference Yamori Y, Horie R, Handa H, Sato M, Fukase M: Spontaneously Hypertensive Rats and Humans. Stroke 1976, 7: 46–53. 10.1161/01.STR.7.1.46PubMed Yamori Y, Horie R, Handa H, Sato M, Fukase M: Spontaneously Hypertensive Rats and Humans. Stroke 1976, 7: 46–53. 10.1161/01.STR.7.1.46PubMed
35.
go back to reference 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.2007.04.015PubMed 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.2007.04.015PubMed
36.
go back to reference 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. 10.1038/jcbfm.1981.6 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. 10.1038/jcbfm.1981.6
37.
go back to reference 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-XPubMed 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-XPubMed
38.
go back to reference 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. 10.1258/002367706775404426PubMed 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. 10.1258/002367706775404426PubMed
39.
go back to reference 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.PubMed 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.PubMed
40.
go back to reference 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.PubMed 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.PubMed
41.
go back to reference 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.2005.02.078PubMed 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.2005.02.078PubMed
42.
go back to reference 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.2005.11.009PubMed 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.2005.11.009PubMed
43.
go back to reference 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.2009.11.007PubMedCentralPubMed 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.2009.11.007PubMedCentralPubMed
44.
go back to reference 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.2010.08.003PubMed 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.2010.08.003PubMed
45.
go back to reference 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.108.533653PubMedCentralPubMed 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.108.533653PubMedCentralPubMed
47.
go back to reference Wieloch T, Nikolich K: Mechanisms of neural plasticity following brain injury. Curr Opin Neurobiol 2006, 16: 258–264. 10.1016/j.conb.2006.05.011PubMed Wieloch T, Nikolich K: Mechanisms of neural plasticity following brain injury. Curr Opin Neurobiol 2006, 16: 258–264. 10.1016/j.conb.2006.05.011PubMed
48.
go back to reference 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.2010.08.026PubMed 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.2010.08.026PubMed
49.
go back to reference 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.27.9.1616PubMed 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.27.9.1616PubMed
50.
go back to reference 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.PubMed 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.PubMed
51.
go back to reference Lipsanen A, Jolkkonen J: Experimental approaches to study functional recovery following cerebral ischemia. Cell Mol Life Sciences 2011, 68: 3007–3017. 10.1007/s00018-011-0733-3 Lipsanen A, Jolkkonen J: Experimental approaches to study functional recovery following cerebral ischemia. Cell Mol Life Sciences 2011, 68: 3007–3017. 10.1007/s00018-011-0733-3
52.
go back to reference 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.a7PubMed 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.a7PubMed
53.
go back to reference 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. 10.1007/s12975-011-0102-4PubMed 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. 10.1007/s12975-011-0102-4PubMed
54.
go back to reference 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/BF02259134PubMed 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/BF02259134PubMed
55.
go back to reference 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.2008.01.031PubMedCentralPubMed 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.2008.01.031PubMedCentralPubMed
56.
go back to reference 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.2006.04.012PubMed 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.2006.04.012PubMed
57.
go back to reference 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. 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.
go back to reference 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.1993.108PubMed 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.1993.108PubMed
59.
go back to reference Kleim JA, Boychuk JA, Adkins DL: Rat models of upper extremity impairment in stroke. ILAR J 2007, 48: 374–384. 10.1093/ilar.48.4.374PubMed Kleim JA, Boychuk JA, Adkins DL: Rat models of upper extremity impairment in stroke. ILAR J 2007, 48: 374–384. 10.1093/ilar.48.4.374PubMed
60.
go back to reference 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.2006.01.014PubMed 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.2006.01.014PubMed
61.
go back to reference 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.410170513PubMed 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.410170513PubMed
62.
go back to reference 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.0000094730.38343.73PubMed 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.0000094730.38343.73PubMed
63.
go back to reference 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/s10571-010-9553-5PubMed 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/s10571-010-9553-5PubMed
64.
go back to reference 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. 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.
go back to reference 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.2006.01.016PubMed 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.2006.01.016PubMed
66.
go back to reference Carmichael ST: Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2005, 2: 396–409. 10.1602/neurorx.2.3.396PubMedCentralPubMed Carmichael ST: Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2005, 2: 396–409. 10.1602/neurorx.2.3.396PubMedCentralPubMed
67.
go back to reference 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)00012-2PubMed 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)00012-2PubMed
68.
go back to reference 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)00259-2PubMed 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)00259-2PubMed
69.
go back to reference 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.xPubMed 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.xPubMed
70.
go back to reference Hossmann K-A: Cerebral ischemia: models, methods and outcomes. Neuropharmacology 2008, 55: 257–270. 10.1016/j.neuropharm.2007.12.004PubMed Hossmann K-A: Cerebral ischemia: models, methods and outcomes. Neuropharmacology 2008, 55: 257–270. 10.1016/j.neuropharm.2007.12.004PubMed
71.
go back to reference 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.20.1.84PubMed 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.20.1.84PubMed
72.
go back to reference 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. 10.1097/00001756-199707280-00040PubMed 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. 10.1097/00001756-199707280-00040PubMed
73.
go back to reference 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.2006.09.027PubMed 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.2006.09.027PubMed
74.
go back to reference 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.0016643PubMedCentralPubMed 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.0016643PubMedCentralPubMed
75.
go back to reference 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.107.495069PubMed 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.107.495069PubMed
76.
go back to reference 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.108.531806PubMed 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.108.531806PubMed
77.
go back to reference 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. 10.1177/1545968307308551PubMedCentralPubMed 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. 10.1177/1545968307308551PubMedCentralPubMed
78.
go back to reference 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.2006.06.035PubMed 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.2006.06.035PubMed
79.
go back to reference 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)00010-7PubMed 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)00010-7PubMed
80.
go back to reference 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.2005.05.070PubMed 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.2005.05.070PubMed
81.
go back to reference 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.2003.06.001PubMed 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.2003.06.001PubMed
82.
go back to reference 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.PubMed 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.PubMed
83.
go back to reference 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.2010.04.025PubMed 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.2010.04.025PubMed
84.
go back to reference Auriat AM, Colbourne F: Delayed rehabilitation lessens brain injury and improves recovery after intracerebral hemorrhage in rats. Brain Res 2009, 1251: 262–268.PubMed Auriat AM, Colbourne F: Delayed rehabilitation lessens brain injury and improves recovery after intracerebral hemorrhage in rats. Brain Res 2009, 1251: 262–268.PubMed
85.
go back to reference 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. 10.1177/1545968311407517PubMed 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. 10.1177/1545968311407517PubMed
86.
go back to reference 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.3834-03.2004PubMed 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.3834-03.2004PubMed
87.
go back to reference 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.PubMed 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.PubMed
88.
go back to reference Hebb D: The Effects of Early Experience on Problem-Solving at Maturity. Am Psychol 1947, 2: 306–307. Hebb D: The Effects of Early Experience on Problem-Solving at Maturity. Am Psychol 1947, 2: 306–307.
89.
go back to reference 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. 10.1177/1545968310372092PubMed 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. 10.1177/1545968310372092PubMed
90.
go back to reference 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.109.572073PubMedCentralPubMed 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.109.572073PubMedCentralPubMed
91.
go back to reference 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.2005.09.027PubMed 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.2005.09.027PubMed
92.
go back to reference 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/y04-013PubMed 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/y04-013PubMed
93.
go back to reference Chopp M, Li Y, Zhang J: Plasticity and remodeling of brain. J Neurol Sci 2008, 265: 97–101. 10.1016/j.jns.2007.06.013PubMed Chopp M, Li Y, Zhang J: Plasticity and remodeling of brain. J Neurol Sci 2008, 265: 97–101. 10.1016/j.jns.2007.06.013PubMed
94.
go back to reference 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.2005.01.004PubMed 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.2005.01.004PubMed
95.
go back to reference Iadecola C, Anrather J: The immunology of stroke: from mechanisms to translation. Nat Med 2011, 17: 796–808. 10.1038/nm.2399PubMedCentralPubMed Iadecola C, Anrather J: The immunology of stroke: from mechanisms to translation. Nat Med 2011, 17: 796–808. 10.1038/nm.2399PubMedCentralPubMed
96.
go back to reference 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.0008101PubMedCentralPubMed 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.0008101PubMedCentralPubMed
97.
go back to reference Schaar KL, Brenneman MM, Savitz SI: Functional assessments in the rodent stroke model. Exp Trans Stroke Med 2010, 2: 13. 10.1186/2040-7378-2-13 Schaar KL, Brenneman MM, Savitz SI: Functional assessments in the rodent stroke model. Exp Trans Stroke Med 2010, 2: 13. 10.1186/2040-7378-2-13
98.
go back to reference 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.xPubMed 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.xPubMed
99.
go back to reference 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.PubMed 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.PubMed
100.
go back to reference 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)00005-8PubMed 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)00005-8PubMed
101.
go back to reference 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)90048-5PubMed 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)90048-5PubMed
102.
go back to reference 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.17.3.472PubMed 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.17.3.472PubMed
103.
go back to reference 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.20.10.1383PubMed 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.20.10.1383PubMed
104.
go back to reference 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. 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.
go back to reference 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)70066-8PubMed 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)70066-8PubMed
106.
go back to reference 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.23.8.1084PubMed 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.23.8.1084PubMed
Metadata
Title
Animal models of post-ischemic forced use rehabilitation: methods, considerations, and limitations
Authors
Jessica M Livingston-Thomas
R Andrew Tasker
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Experimental & Translational Stroke Medicine / Issue 1/2013
Electronic ISSN: 2040-7378
DOI
https://doi.org/10.1186/2040-7378-5-2

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