Assessing post-stroke behavior in mouse models of focal ischemia

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 3, 2013, Pages 330-338

  Balkaya, Mustafa ^a,b   Kröber, Jan M ^a   Rex, Andre ^a   Endres, Matthias ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

behavior; focal ischemia; functional outcome; sensory motor tests; stroke

Indexed keywords

ADHESIVE REMOVAL TEST; ANIMAL BEHAVIOR; ARTICLE; BEHAVIOR; BRAIN ISCHEMIA; BRAIN SIZE; CEREBROVASCULAR ACCIDENT; CORNER TEST; CYLINDER TEST; EXPERIMENTAL TEST; FOOT FAULT TEST; GAIT; GOOD LABORATORY PRACTICE; GRIP STRENGTH; HANDEDNESS; LADDER RUNG TEST; LATENT PERIOD; NONHUMAN; OPEN FIELD BEHAVIOR; OPEN FIELD TEST; OUTCOME ASSESSMENT; PERSONAL EXPERIENCE; PHENOTYPE; POLE TEST; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; ROTAROD TEST; SENSORIMOTOR FUNCTION; STAIRCASE TEST; TRAUMATIC BRAIN INJURY;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; HUMANS; MICE; STROKE;

EID: 84874667813     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2012.185     Document Type: Article

References (75)

1. Endres M, Engelhardt B, Koistinaho J, Lindvall O, Meairs S, Mohr JP et al. Improving outcome after stroke: overcoming the translational roadblock. Cerebrovasc Dis 2008; 25: 268-278.
2. Sena E, van der Worp HB, Howells D, Macleod M. How can we improve the pre-clinical development of drugs for strokeTrends Neurosci 2007; 30: 433-439.
3. Hattori K, Lee H, Hurn PD, Crain BJ, Traystman RJ, DeVries AC. Cognitive deficits after focal cerebral ischemia in mice. Stroke 2000; 31: 1939-1944.
4. Bouet V, Freret T, Toutain J, Divoux D, Boulouard M, Schumann-Bard P. Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp Neurol 2007; 203: 555-567.
5. Freret T, Bouet V, Leconte C, Roussel S, Chazalviel L, Divoux D et al. Behavioral deficits after distal focal cerebral ischemia in mice: Usefulness of adhesive removal test. Behav Neurosci 2009; 123: 224-230.
6. Hunter AJ, Hatcher J, Virley D, Nelson P, Irving E, Hadingham SJ et al. Functional assessments in mice and rats after focal stroke. Neuropharmacology 2000; 39: 806-816.
7. Zhang L, Chen J, Li Y, Zhang ZG, Chopp M. Quantitative measurement of motor and somatosensory impairments after mild (30 min) and severe (2 h) transient middle cerebral artery occlusion in rats. J Neurol Sci 2000; 174: 141-146.
8. Markgraf CG, Green EJ, Watson B, McCabe PM, Schneiderman N, Dietrich WD et al. Recovery of sensorimotor function after distal middle cerebral artery photothrombotic occlusion in rats. Stroke 1994; 25: 153-159.
9. STAIR. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 1999; 30: 2752-2758.
10. Bonthuis PJ, Cox KH, Searcy BT, Kumar P, Tobet S, Rissman EF. Of mice and rats: key species variations in the sexual differentiation of brain and behavior. Front Neuroendocrinol 2010; 31: 341-358.
11. Kuroda S, Tsuchidate R, Smith ML, Maples KR, Siesjo BK. Neuroprotective effects of a novel nitrone, NXY-059, after transient focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 1999; 19: 778-787.
12. 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.
13. Li X, Blizzard KK, Zeng Z, DeVries AC, Hurn PD, McCullough LD. Chronic behavioral testing after focal ischemia in the mouse: functional recovery and the effects of gender. Exp Neurol 2004; 187: 94-104.
14. Boleij H, Salomons AR, van Sprundel M, Arndt SS, Ohl F. Not all mice are equal: welfare implications of behavioural habituation profiles in four 129 mouse substrains. PLoS ONE 2012; 7: e42544.
15. Maeda K, Hata R, Hossmann KA. Regional metabolic disturbances and cerebrovascular anatomy after permanent middle cerebral artery occlusion in C57black/6 and SV129 mice. Neurobiol Dis 1999; 6: 101-108.
16. Fahlstrom A, Zeberg H, Ulfhake B. Changes in behaviors of male C57BL/6J mice across adult life span and effects of dietary restriction. Age (Dordr) 2011; 34: 1435-1452.
17. Sweetnam D, Holmes A, Tennant KA, Zamani A, Walle M, Jones P et al. Diabetes impairs cortical plasticity and functional recovery following ischemic stroke. J Neurosci 2012; 32: 5132-5143.
18. Sieber MW, Claus RA, Witte OW, Frahm C. Attenuated inflammatory response in aged mice brains following stroke. PLoS ONE 2011; 6: e26288.
19. Popa-Wagner A, Buga AM, Kokaia Z. Perturbed cellular response to brain injury during aging. Ageing Res Rev 2011; 10: 71-79.
20. Manwani B, Liu F, Xu Y, Persky R, Li J, McCullough LD. Functional recovery in aging mice after experimental stroke. Brain Behav Immun 2011; 25: 1689-1700.
21. Da Silva Costa-Aze V, Dauphin F, Boulouard M. Serotonin 5-HT6 receptor blockade reverses the age-related deficits of recognition memory and working memory in mice. Behav Brain Res 2011; 222: 134-140.
22. Crawley JN. What's Wrong with My Mouse: Behavioral Phenotyping of Transgenic and Knockout Mice. Wiley-Liss, 2000.
23. Ferrara A, El Bejaoui S, Seyen S, Tirelli E, Plumier JC. The usefulness of operant conditioning procedures to assess long-lasting deficits following transient focal ischemia in mice. Behav Brain Res 2009; 205: 525-534.
24. Hayakawa K, Nakano T, Irie K, Higuchi S, Fujioka M, Orito K et al. Inhibition of reactive astrocytes with fluorocitrate retards neurovascular remodeling and recovery after focal cerebral ischemia in mice. J Cereb Blood Flow Metab 2010; 30: 871-882.
25. Wang X, Xu L, Wang H, Zhan Y, Pure E, Feuerstein GZ. CD44 deficiency in mice protects brain from cerebral ischemia injury. J Neurochem 2002; 83: 1172-1179.
26. Jin K, Wang X, Xie L, Mao XO, Greenberg DA. Transgenic ablation of doublecortinexpressing cells suppresses adult neurogenesis and worsens stroke outcome in mice. Proc Natl Acad Sci USA 2010; 107: 7993-7998.
27. Li Y, Chopp M, Chen J, Wang L, Gautam SC, Xu YX et al. Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J Cereb Blood Flow Metab 2000; 20: 1311-1319.
28. Lee JK, Park MS, Kim YS, Moon KS, Joo SP, Kim TS et al. Photochemically induced cerebral ischemia in a mouse model. Surg Neurol 2007; 67: 620-625, discussion 625.
29. Guo Q, Wang G, Liu X, Namura S. Effects of gemfibrozil on outcome after permanent middle cerebral artery occlusion in mice. Brain Res 2009; 1279: 121-130.
30. Dunham NW, Miya TS. A note on a simple apparatus for detecting neurological deficit in rats and mice. J Am Pharm Assoc Am Pharm Assoc (Baltim) 1957; 46: 208-209.
31. Jones BJ, Roberts DJ. A rotarod suitable for quantitative measurements of motor incoordination in naive mice. Naunyn Schmiedebergs Arch Exp Pathol Pharmakol 1968; 259: 211.
32. Homanics GE, Quinlan JJ, Firestone LL. Pharmacologic and behavioral responses of inbred C57BL/6J and strain 129/SvJ mouse lines. Pharmacol Biochem Behav 1999; 63: 21-26.
33. Ji S, Kronenberg G, Balkaya M, Farber K, Gertz K, Kettenmann H et al. Acute neuroprotection by pioglitazone after mild brain ischemia without effect on longterm outcome. Exp Neurol 2009; 216: 321-328.
34. Royl G, Balkaya M, Lehmann S, Lehnardt S, Stohlmann K, Lindauer U et al. Effects of the PDE5-inhibitor vardenafil in a mouse stroke model. Brain Res 2009; 1265: 148-157.
35. Prinz V, Laufs U, Gertz K, Kronenberg G, Balkaya M, Leithner C et al. Intravenous rosuvastatin for acute stroke treatment: an animal study. Stroke 2008; 39: 433-438.
36. Winter B, Juckel G, Viktorov I, Katchanov J, Gietz A, Sohr R et al. Anxious and hyperactive phenotype following brief ischemic episodes in mice. Biol Psychiatry 2005; 57: 1166-1175.
37. Ogawa N, Hirose Y, Ohara S, Ono T, Watanabe Y. A simple quantitative bradykinesia test in MPTP-treated mice. Res Commun Chem Pathol Pharmacol 1985; 50: 435-441.
38. Gertz K, Priller J, Kronenberg G, Fink KB, Winter B, Schrock H et al. Physical activity improves long-term stroke outcome via endothelial nitric oxide synthasedependent augmentation of neovascularization and cerebral blood flow. Circ Res 2006; 99: 1132-1140.
39. Abe T, Kunz A, Shimamura M, Zhou P, Anrather J, Iadecola C. The neuroprotective effect of prostaglandin E2 EP1 receptor inhibition has a wide therapeutic window, is sustained in time and is not sexually dimorphic. J Cereb Blood Flow Metab 2009; 29: 66-72.
40. Broughton BR, Brait VH, Guida E, Lee S, Arumugam TV, Gardiner-Mann CV et al. Stroke increases G protein-coupled estrogen receptor expression in the brain of male but not female mice. Neurosignals 2012 (e-pub ahead of print).
41. De Silva TM, Brait VH, Drummond GR, Sobey CG, Miller AA. Nox2 oxidase activity accounts for the oxidative stress and vasomotor dysfunction in mouse cerebral arteries following ischemic stroke. PLoS ONE 2011; 6: e28393.
42. Zhang L, Schallert T, Zhang ZG, Jiang Q, Arniego P, Li Q et al. A test for detecting long-term sensorimotor dysfunction in the mouse after focal cerebral ischemia. J Neurosci Methods 2002; 117: 207-214.
43. Hao J, Mdzinarishvili A, Abbruscato TJ, Klein J, Geldenhuys WJ, Van der Schyf CJ et al. Neuroprotection in mice by NGP1-01 after transient focal brain ischemia. Brain Res 2008; 1196: 113-120.
44. Chen J, Zhang C, Jiang H, Li Y, Zhang L, Robin A et al. Atorvastatin induction of VEGF and BDNF promotes brain plasticity after stroke in mice. J Cereb Blood Flow Metab 2005; 25: 281-290.
45. Lubjuhn J, Gastens A, von Wilpert G, Bargiotas P, Herrmann O, Murikinati S et al. Functional testing in a mouse stroke model induced by occlusion of the distal middle cerebral artery. J Neurosci Methods 2009; 184: 95-103.
46. Tennant KA, Jones TA. Sensorimotor behavioral effects of endothelin-1 induced small cortical infarcts in C57BL/6 mice. J Neurosci Methods 2009; 181: 18-26.
47. Schallert T, Upchurch M, Lobaugh N, Farrar SB, Spirduso WW, Gilliam P et al. Tactile extinction: distinguishing between sensorimotor and motor asymmetries in rats with unilateral nigrostriatal damage. Pharmacol Biochem Behav 1982; 16: 455-462.
48. Schallert T, Upchurch M, Wilcox RE, Vaughn DM. Posture-independent sensorimotor analysis of inter-hemispheric receptor asymmetries in neostriatum. Pharmacol Biochem Behav 1983; 18: 753-759.
49. Leconte C, Tixier E, Freret T, Toutain J, Saulnier R, Boulouard M et al. Delayed hypoxic postconditioning protects against cerebral ischemia in the mouse. Stroke 2009; 40: 3349-3355.
50. Balkaya M, Kro ber J, Gertz K, Peruzzaro S, Endres M. Characterization of long-term functional outcome in a murine model of mild brain ischemia. (unpublished data).
51. Denes A, Ferenczi S, Halasz J, Kornyei Z, Kovacs KJ. Role of CX3CR1 (fractalkine receptor) in brain damage and inflammation induced by focal cerebral ischemia in mouse. J Cereb Blood Flow Metab 2008; 28: 1707-1721.
52. Rehni AK, Singh N, Jaggi AS, Singh M. Amniotic fluid derived stem cells ameliorate focal cerebral ischaemia-reperfusion injury induced behavioural deficits in mice. Behav Brain Res 2007; 183: 95-100.
53. Crawley JN. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 1985; 9: 37-44.
54. Belzung C, Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 2001; 125: 141-149.
55. Li J, Henman MC, Tatlisumak T, Shaw GG, Doyle KM. The pre-ischaemic neuroprotective effects of N1-dansyl-spermine in a transient focal cerebral ischaemia model in mice. Brain Res 2005; 1055: 180-185.
56. Kilic E, Kilic U, Bacigaluppi M, Guo Z, Abdallah NB, Wolfer DP et al. Delayed melatonin administration promotes neuronal survival, neurogenesis and motor recovery, and attenuates hyperactivity and anxiety after mild focal cerebral ischemia in mice. J Pineal Res 2008; 45: 142-148.
57. Prut L, Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 2003; 463: 3-33.
58. van de Port IG, Wood-Dauphinee S, Lindeman E, Kwakkel G. Effects of exercise training programs on walking competency after stroke: a systematic review. Am J Phys Med Rehabil 2007; 86: 935-951.
59. Nadeau S, Duclos C, Bouyer L, Richards CL. Guiding task-oriented gait training after stroke or spinal cord injury by means of a biomechanical gait analysis. Prog Brain Res 2011; 192: 161-180.
60. Belda-Lois JM, Mena-del Horno S, Bermejo-Bosch I, Moreno JC, Pons JL, Farina D et al. Rehabilitation of gait after stroke: a review towards a top-down approach. J Neuroeng Rehabil 2011; 8: 66.
61. de Medinaceli L, Freed WJ, Wyatt RJ. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol 1982; 77: 634-643.
62. Inserra MM, Bloch DA, Terris DJ. Functional indices for sciatic, peroneal, and posterior tibial nerve lesions in the mouse. Microsurgery 1998; 18: 119-124.
63. Wang Y, Bontempi B, Hong SM, Mehta K, Weinstein PR, Abrams GM et al. A comprehensive analysis of gait impairment after experimental stroke and the therapeutic effect of environmental enrichment in rats. J Cereb Blood Flow Metab 2008; 28: 1936-1950.
64. Arsenijevic D, de Bilbao F, Plamondon J, Paradis E, Vallet P, Richard D et al. Increased infarct size and lack of hyperphagic response after focal cerebral ischemia in peroxisome proliferator-activated receptor beta-deficient mice. J Cereb Blood Flow Metab 2006; 26: 433-445.
65. Hetze S, Romer C, Teufelhart C, Meisel A, Engel O. Gait analysis as a method for assessing neurological outcome in a mouse model of stroke. J Neurosci Methods 2012; 206: 7-14.
66. 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.
67. Collins RL. On the inheritance of handedness. I. Laterality in inbred mice. J Hered 1968; 59: 9-12.
68. 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.
69. Baird AL, Meldrum A, Dunnett SB. The staircase test of skilled reaching in mice. Brain Res Bull 2001; 54: 243-250.
70. Gibson CL, Bath PM, Murphy SP. G-CSF reduces infarct volume and improves functional outcome after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 2005; 25: 431-439.
71. Wang X, Liu J, Zhu H, Tejima E, Tsuji K, Murata Y et al. Effects of neuroglobin overexpression on acute brain injury and long-term outcomes after focal cerebral ischemia. Stroke 2008; 39: 1869-1874.
72. Farr TD, Liu L, Colwell KL, Whishaw IQ, Metz GA. Bilateral alteration in stepping pattern after unilateral motor cortex injury: a new test strategy for analysis of skilled limb movements in neurological mouse models. J Neurosci Methods 2006; 153: 104-113.
73. 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.
74. Macleod MR, Fisher M, O'Collins V, Sena ES, Dirnagl U, Bath PM et al. Good laboratory practice: preventing introduction of bias at the bench. Stroke 2009; 40: e50-e52.
75. Holmes A, Wrenn CC, Harris AP, Thayer KE, Crawley JN. Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice. Genes Brain Behav 2002; 1: 55-69.