Rat models of upper extremity impairment in stroke

ILAR Journal

Volumn 48, Issue 4, 2007, Pages 374-384

  Kleim, Jeffrey A ^a,b   Boychuk, Jeffery A ^a   Adkins, DeAnna L ^b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Forelimb; Impairment; Ischemia; Middle cerebral artery; Rat; Stroke

Indexed keywords

BRAIN HEMORRHAGE; BRAIN ISCHEMIA; CONVALESCENCE; DISABILITY; FORELIMB; HUMAN; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NONHUMAN; REVIEW; SENSORIMOTOR CORTEX; STROKE; SURVIVAL; THROMBOSIS; VASOCONSTRICTION; ANIMAL; ARM; BEHAVIOR; CEREBRAL ARTERY DISEASE; CEREBROVASCULAR ACCIDENT; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; METHODOLOGY; PATHOPHYSIOLOGY; RAT;

ANIMALIA; RATTUS;

ENDOTHELIN 1;

ANIMALS; BEHAVIORAL SYMPTOMS; CEREBROVASCULAR ACCIDENT; DISEASE MODELS, ANIMAL; ENDOTHELIN-1; INFARCTION, MIDDLE CEREBRAL ARTERY; RATS; RESEARCH DESIGN; UPPER EXTREMITY;

EID: 36048987417     PISSN: 10842020     EISSN: None     Source Type: Journal    
DOI: 10.1093/ilar.48.4.374     Document Type: Review

References (83)

1. Adkins DL, Jones TA. 2005. D-amphetamine enhances skilled reaching after ischemic cortical lesions in rats. Neurosci Lett 380:214-218.
2. Ballermann M, Tompkins G, Whishaw IQ. 2000. Skilled forelimb reaching for pasta guided by tactile input in the rat as measured by accuracy, spatial adjustments, and force. Behav Brain Res 109:49-57.
3. Ballermann M, Metz GA, McKenna JE, Klassen F, Whishaw IQ. 2001. The pasta matrix reaching task: A simple test for measuring skilled reaching distance, direction, and dexterity in rats. J Neurosci Methods 106:39-45.
4. Barth T, Jones TA, Schallert T. 1990. Functional subdivisions of the rat sensorimotor cortex. Behav Brain Res 39:73-95.
5. Biernaskie J, Corbett D. 2001. Enriched rehabilitation training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci 21:5272-5280.
6. Biernaskie J, Chernenko G, Corbett D. 2004. Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. J Neurosci 24:1245-1254.
7. Biernaskie J, Szymanska A, Windle V, Corbett D. 2005. Bi-hemispheric contribution to functional motor recovery of the affected forelimb following focal ischemic brain injury in rats. Eur J Neurosci 21:989-999.
8. Bland S, Pillai R, Aronowski J, Grotta J, Schallert T. 2001. Early overuse and disuse of the affected forelimb after moderately severe intraluminal suture occlusion of the middle cerebral artery in rats. Behav Brain Res 126:33-41.
9. Butovas S, Lukkarinen J, Virtanen T, Jolkkonen J, Sivenius J. 2001. Differential effect of the alpha2-adrenoceptor antagonist, atipamezole, in limb placing task and skilled forepaw use following experimental stroke. Restor Neurol Neurosci 18:143-151.
10. Carmichael S. 2005. Rodent models of focal stroke: Size, mechanism, and purpose. NeuroRx 2:396-409.
11. Cenci M, Whishaw IQ, Schallert T. 2002. Animal models of neurological deficits: How relevant is the rat? Nature 3:874-879.
12. Cramer S. 2003. Clinical issues in animal models of stroke and rehabilitation. ILAR J 44:83-84.
13. DeBow SB, Clark DL, MacLellan C, Colbourne F. 2003. Incomplete assessment of experimental cytoprotectants: A survey of recent practices in rodent ischemia studies. Can J Neurol Sci 30:368-374.
14. Del Bigio MR, Yan HJ, Buist R, Peeling J. 1996. Experimental intracerebral hemorrhage in rats: Magnetic resonance imaging and histopathological correlates. Stroke 27:2312-2319.
15. Dittmar M, Spruss T, Schuierer G, Horn M. 2003. External carotid artery territory ischemia impairs outcome in the endovascular filament model of middle cerebral artery occlusion in rats. Stroke 34:2252-2257.
16. Duncan P, Lai S, Keighly J. 2000. Defining post-stroke recovery: Implications for design and interpretation of drug trials. Neuropharmacology 39:835-841.
17. Duverger D, MacKenzie ET. 1988. The quantification of cerebral infarction following focal ischemia in the rat: Influence of strain, arterial pressure, blood glucose concentration, and age. J Cereb Blood Flow Metab 8:449-461.
18. Erdo F, Berzsenyi P, Nemet L, Andrasi F. 2006. Talampanel improves the functional deficit after transient focal cerebral ischemia in rats: A 30-day follow up study. Brain Res Bull 68:269-276.
19. Eshkol N, Wachman A. 1958. Movement Notation. London: Weidenfeld and Nicolson.
20. Frost S, Barbay S, Mumert M, Stowe A, Nudo R. 2006. An animal model of capsular infarct: Endothelin-1 injections in the rat. Behav Brain Res 169:206-211.
21. Fuxe K, Bjelke B, Andbjer B, Grahn H, Rimondini R, Agnati L. 1997. Endothelin-1 induced lesions of the fronto-parietal cortex of the rat: A possible model of focal cortical ischemia. NeuroReport 8:2623-2629.
22. Garcia J, Liu K, Ho K. 1995. Neuronal necrosis after middle cerebral artery occlusion in Wistar rats progresses at different time intervals in the caudoputamen and the cortex. Stroke 26:636-642.
23. Gerriets T, Li F, Silva M, Meng X, Brevard M, Sotak C, Fisher M. 2003. The macrosphere model: Evaluation of a new stroke model for permanent middle cerebral artery occlusion in rats. J Neurosci Methods 122: 201-211.
24. Gharbawie OA, Gonzalez C, Whishaw IQ. 2005a. Skilled reaching impairments from the lateral frontal cortex component of middle cerebral artery stroke: A qualitative and quantitative comparison to focal motor cortex lesions in rats. Behav Brain Res 156:125-137.
25. Gharbawie OA, Gonzalez CL, Williams PT, Kleim JA, Whishaw IQ. 2005b. Middle cerebral artery (MCA) stroke produces dysfunction in adjacent motor cortex as detected by intracortical microstimulation in rats. Neuroscience 130:601-610.
26. Gharbawie OA, Whishaw IQ. 2006. Parallel stages of learning and recovery of skilled reaching after motor cortex stroke: "Oppositions" organize normal and compensatory movements. Behav Brain Res 175: 249-262.
27. Gilmour G, Iverson S, O'Neill M, Bannerman D. 2004. The effects of intracortical endothelin-1 injections on skilled forelimb use: Implications for modeling recovery function after stroke. Behav Brain Res 150:171-183.
28. Gilmour G, Iverson S, O'Neill MF, O'Neill MJ, Ward M, Bannerman D. 2005. Amphetamine promotes task-dependent recovery following focal cortical ischemic lesions in the rat. Behav Brain Res 165:98-109.
29. Gonzalez C, Kolb B. 2003. A comparison of different models of stroke on behaviour and brain morphology. Eur J Neurosci 18:1950-1962.
30. Gonzalez C, Gharbawie OA, Kolb B. 2006. Chronic low-dose administration of nicotine facilitates recovery and synaptic change after focal ischemia in rats. Neuropharmacology 50:777-787.
31. Grabowski M, Brundin P, Johansson B. 1993. Paw-reaching, sensorimotor, and rotational behavior after brain infarction in rats. Stroke 24:889-895.
32. Gresham G, Kelly-Hayes M, Wolf P, Beiser A, Kase C, D'Agostino R. 1995. Survival and functional status of 20 or more years after first stroke: The Framingham study. Stroke 29:793-797.
33. Hernandez T, Schallert T. 1988. Seizures and recovery from experimental brain damage. Exp Neurol 102:318-324.
34. Hewlett K, Corbett D. 2006. Delayed minocycline treatment reduces long-term functional deficits and histological injury in a rodent model of focal ischemia. Neuroscience 141:27-33.
35. Hsu JE, Jones TA. 2006. Contralesional neural plasticity and functional changes in the less-affected forelimb after large and small cortical infarcts in rats. Exp Neurol 201:479-494.
36. Jones TA, Schallert T. 1992. Subcortical deterioration after cortical damage: Effects of diazepam and relation to recovery of function. Behav Brain Res 51:1-13.
37. Jones TA, Bury SD, Adkins-Muir DL, Luke LM, Allied RP, Sakata JT. 2003. Importance of behavioral manipulations and measure in rat models of brain damage and brain repair. ILAR J 44:144-152.
38. Kanemitsu H, Nakagomi T, Tamura A, Tsuchiya T, Kono G, Sano K. 2002. Differences in the extent of primary ischemic damage between middle cerebral artery coagulation and intraluminal occlusion models. J Cereb Blood Flow Metab 22:1196-1204.
39. Kleim JA, Bruneau R, Vandeberg P, MacDonald E, Mulrooney R, Pocock D. 2003. Motor cortex stimulation enhances motor recovery and reduces peri-infarct dysfunction following ischemic insult. Neurol Res 25:789-793.
40. Kleim JA, Jones TA. 2007. Experience-dependent neural plasticity: Implications for rehabilitation. J Speech Hearing Lang Res (In Press).
41. Kolb B, Whishaw IQ. 1983. Dissociation of the contributions of the prefrontal, motor, and parietal cortex to the control of movement in the rat: An experimental review. Can J Psychol 37:211-232.
42. Kolb B, Morshead C, Gonzalez C, Kim M, Gregg C, Shingo T, Weiss S. 2007. Growth factor-stimulated generation of new cortical tissue and functional recovery after stroke damage to the motor cortex of rats. J Cereb Blood Flow Metab 27:983-997.
43. Kozuimi J, Yoshida Y, Nakazawa T, Ooneda G. 1986. Experimental studies of ischemic brain edema. 1. A new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area. Jpn J Stroke 8:1-8.
44. Lindner M, Gribkoff V, Donlan N, Jones TA. 2003. Long-lasting functional disabilities in middle-aged rats with small cerebral infarcts. J Neurosci 23:10913-10922.
45. Lyden PD, Zivin JA. 1993. Hemorrhagic transformation after cerebral ischemia: Mechanisms and incidence. J Cereb Blood Flow Metab 5.1-16.
46. MacLellan CL, Girgis J, Colbourne F. 2004. Delayed onset of prolonged hypothermia improves outcome after intracerebral hemorrhage in rats. J Cereb Blood Flow and Metab 24:432-440.
47. MacLellan CL, Gyawali S, Colbourne F. 2006. Skilled reaching impairments follow intrastriatal hemorrhagic stroke in rats. Behav Brain Res 175:82-90.
48. Macrae I, Robinson M, Graham D, Reid J, McCulloch J. 1993. Endothelin-1-induced reductions in cerebral blood flow: Dose dependency, time course, and neuropathological consequences. J Cereb Blood Flow Metab 13:276-284.
49. McColl B, Carswell H, McCulloch J, Horsburgh K. 2004. Extension of cerebral hypoperfusion and ischaemic pathology beyond MCA territory after intraluminal filament occlusion in C57BI/6J mice. Brain Res 997: 15-23.
50. Metz G, Whishaw IQ. 2000. Skilled reaching an action pattern: Stability in rat (Rattus norvegicus) grasping movements as a function of changing food pellet size. Behav Brain Res 116:111-122.
51. Metz G, Whishaw IQ. 2002. Cortical and subcortical lesions impair skilled walking in the ladder rung test: A new task to evaluate fore- and hindlimb stepping, placing, and co-ordination. J Neurosci Methods 115:169-179.
52. Montoya C, Campbell-Hope L, Pemberton K, Dunnett S. 1991. The "stair-case test": A measure of independent forelimb reaching and grasping abilities in rats. J Neurosci Methods 36:2-3.
53. Nakagomi S, Kiryu-Seo S, Kiyama H. 2000. Endothelin-converting enzymes and endothelin receptor B messenger RNAs are expressed in different neural cell species and these messenger RNAs are coordinately induced in neurons and astrocytes respectively following nerve injury. Neuroscience 101:441-449.
54. O'Bryant A, Bernier B, Jones TA. 2007. Abnormalities in skilled reaching movements are improved by peripheral anesthetization of the less-affected forelimb after sensorimotor cortical infarcts in rats. Behav Brain Res 177:298-307.
55. Palmer G, Peeling J, Corbett D, Del Bigio M, Hudzik T. 2001. T2-weighted MRI correlates with long-term histopathology, neurology scores, and skilled motor behavior in a rat stroke model. Ann N Y Acad Sci 939:283-296.
56. Papadopoulos C, Tsai S, Alsbiei T, O'Brien T, Schwab M, Kartje G. 2002. Functional recovery and neuroanatomical plasticity following middle cerebral artery occlusion and IN-1 antibody treatment in the adult rat. Ann Neurol 51:433-441.
57. Pitsikas N, Brambilla A, Besozzi C, Bonali P, Fodritto F, Grippa N, Scandroglio A, Borsini F. 2001. Effects of cerestat and NBQX on functional and morphological outcomes in rat focal cerebral ischemia. Pharmacol Biochem Behav 68:443-447.
58. Riek-Burchardt M, Henrich-Noack P, Metz G, Reymann K. 2004. Detection of chronic sensorimotor impairments in the ladder rung walking task in rats with endothelin-1-induced mild focal ischemia. J Neuro Methods 137:227-233.
59. Roof RL, Schielke GP, Ren X, Hall ED. 2001. A comparison of long-term functional outcome after 2 middle cerebral artery occlusion models in rats. Stroke 32: 2648-2657.
60. Rosenberg GA, Mun-Bryce S, Wesley M, Kornfeld M. 1990. Collagenase-induced intracerebral hemorrhage in rats. Stroke 21:801-807.
61. Schallert TA, Fleming S, Leasure J, Tillerson J, Bland S. 2000. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39:777-787.
62. Schallert T, Whishaw IQ. 1984. Bilateral cutaneous stimulation of the somatosensory system in hemidecorticate rats. Behav Neurosci 98:518-540.
63. Schallert T, Woodlee MT. 2005. Orienting and placing. In: Whishaw IQ, Kolb B, eds. The Behavior of the Laboratory Rat: A Handbook with Tests. New York: Oxford University Press. p 129-140.
64. Seymour A, Andrews E, Tsai S, Markus T, Bollnow M, Brenneman M, O'Brien T, Castro A, Schwab M, Kartje G. 2005. Delayed treatment with monoclonal antibody IN-1 1 week after stroke results in recovery of function and corticorubral plasticity in adult rats. J Cereb Blood Flow Metab 10:1366-1375.
65. Shanina E, Schallert T, Witte O, Redecker C. 2006. Behavioral recovery from unilateral photothrombotic infarcts of the forelimb sensorimotor cortex in rats: Role of the contralateral cortex. Neuroscience 139:1495-1506.
66. Sharkey J, Ritchie I, Kelly P. 1993. Perivascular microapplication of endothelin-1: A new model of focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 13:865-871.
67. Sharkey J, Butcher S. 1995. Characterisation of an experimental model of stroke produced by intracerebral microinjection of endothelin-1 adjacent to the rat middle cerebral artery. J Neurosci Methods 60:125-131.
68. Stroemer R, Kent T, Hulsebosch C. 1995. Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke 26:2135-2144.
69. Stroemer R, Kent T, Hulsebosch C. 1998. Enhanced neocortical neural sprouting, synaptogenesis, and behavioral recovery with D-amphetamine therapy after neocortical infarction in rats. Stroke 29:2381-2393.
70. Teskey CG, Flynn C, Goertzen C, Monfils M, Young N. 2003. Cortical stimulation improves skilled forelimb use following a focal ischemic infarct in the rat. Neurol Res 25:794-800.
71. Wang C, Todd K, Yang Y, Gordon T, Shuaiob A. 2001. Patency of cerebral microvessels after focal embolic stroke in the rat. J Cereb Blood Flow Metab 21:413-421.
72. Watson B, Dietrich W, Busto R, Wachtel M, Ginsberg M. 1985. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol 17:497-504.
73. Whishaw IQ, Pellis S. 1990. The structure of skilled forelimb reaching in the rat: A proximally driven movement with a single distal rotatory component. Behav Brain Res 41:49-59.
74. Whishaw IQ, Pellis S, Gorny B, Kolb B, Tetzlaff W. 1993. Proximal and distal impairments in rat forelimb use in reaching follow unilateral pyramidal tract lesions. Behav Brain Res 56:59-76.
75. Whishaw IQ, Sarna J, Pellis S. 1998. Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behav Brain Res 96:79-91.
76. Whishaw IQ, Suchowersky O, Davis L, Sarna J, Metz G, Pellis S. 2002. 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 133:165-176.
77. Windle V, Corbett D. 2005, Fluoxetine and recovery of motor function after focal ischemia in rats. Brain Res 1044:25-32.
78. Windle V, Szymanska A, Granter-Button S, White C, Buist R, Peeling J, Corbett D. 2006. An analysis of four different methods of producing focal cerebral ischemia with endothelin-1 in the rat. Exp Neurol 201: 324-334.
79. Woodlee M, Asseo-Garcia A, Zhao X, Liu S, Jones TA, Schallert T. 2005. Testing forelimb placing "across the midline" reveals distinct, lesion-dependent patterns of recovery in rats. Exp Neurol 191:310-317.
80. Xue M, Del Bigio MR. 2000. Intracerebral injection of autologous whole blood in rats: Time course of inflammation and cell death. Neurosci Lett 283:230-232.
81. Yager J, Wright S, Armstrong E, Jahraus C, Saucier D. 2006. The influence of aging on recovery following ischemic brain damage. Behav Brain Res 173:171-180.
82. Zhang Z, Chopp M, Zhang R, Goussev A. 1997. A mouse model of embolic focal cerebral ischemia. J Cereb Blood Flow Metab 17:1081-1088.
83. Zhao C, Puurunen K, Schallert T, Sivenius J, Jolkkonen J. 2005. Effect of cholinergic medication, before and after focal photothrombotic ischemic cortical injury, on histological and functional outcome in aged and young adult rats. Behav Brain Res 156:85-94.