Motor balance and coordination training enhances functional outcome in rat with transient middle cerebral artery occlusion

Neuroscience

Volumn 123, Issue 3, 2004, Pages 667-674

  Ding, Y ^a   Li, J ^a   Lai, Q ^b   Rafols, J A ^a   Luan, X ^a   Clark, J ^a,c   Diaz, F G ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Functional recovery; Motor behavior tasks; Motor training; Rota rod; Stroke; Treadmill

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; COORDINATION; EVALUATION; LOCOMOTION; MALE; MEASUREMENT; MIDDLE CEREBRAL ARTERY; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR PERFORMANCE; NONHUMAN; PARIETAL LOBE; PRIORITY JOURNAL; RAT; TRAINING; TREADMILL EXERCISE; TREATMENT OUTCOME;

EID: 0346099205     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2003.08.031     Document Type: Article

References (67)

1. Barth T.M., Jones T.A., Schallert T. Functional subdivisions of the rat somatic sensorimotor cortex. Behav Brain Res. 39:1990;73-95.
2. Black J.E., Isaacs K.R., Anderson B.J., Alcantara A.A., Greenough W.T. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci USA. 87:1990;5568-5572.
3. Borlongan C.V. Motor activity-mediated partial recovery in ischemic rats. Neuroreport. 11:2000;4063-4067.
4. Borlongan C.V., Cahill D.W., Sanberg P.R. Locomotor and passive avoidance deficits following occlusion of the middle cerebral artery. Physiol Behav. 58:1995;909-917.
5. Campbell C.A., Hunter A.J. Preclinical models of stroke. Miller L.P. Stroke therapy: basic, preclinical, and clinical directions. 1999;39-61 Wiley-Liss, Inc, New York.
6. Chugani H., Muller R., Chugani D. Functional brain reorganization in children. Brain Dev. 18:1996;347-356.
7. Colle L.M., Holmes L.J., Pappius H.M. Correlation between behavioral status and cerebral glucose utilization in rats following freezing lesion. Brain Res. 397:1986;27-36.
8. Dahlqvist P., Zhao L., Johansson I.M., Mattsson B., Johansson B.B., Seckl J.R., Olsson T. Environmental enrichment alters nerve growth factor-induced gene A and glucocorticoid receptor messenger RNA expression after middle cerebral artery occlusion in rats. Neuroscience. 93:1999;527-535.
9. Ding Y., Yao B., Lai Q., McAllister J.P. II. Impaired motor learning and diffuse axonal damage in motor and visual systems of the rat following traumatic brain injury. Neurol Res. 23:2001;193-202.
10. Ding Y, Zhou Y, Li J, Lai Q, Diaz FG (2001b) Long term neuroprotective effect of inhibiting poly (ADP-ribose) polymerase in rats with middle cerebral artery occlusion using a behavioral assessment. Brain Res 210-217.
11. Ding Y., Zhou Y., Li J., Lai Q., Diaz F.G. Impaired motor activity and motor learning function in rat with middle cerebral artery occlusion. Behav Brain Res. 132:2002;29-36.
12. Ding Y., Li J., Clark J., Diaz F.G., Rafols J.A. Synaptic plasticity in thalamic nuclei enhanced by motor skill training in rat with transient middle cerebral artery occlusion. Neurol Res. 25:2003;189-194.
13. Ding Y., Li J., Lai Q., Azam S., Rafols J.A., Diaz F.G. Functional improvement after motor training is correlated with synaptic plasticity in rat thalamus. Neurol Res. 24:2002;829-836.
14. Ding Y., Li J., Rafols J.A., Clark J., Phillis J.W., Diaz F.G. Pre-ischemic motor exercise reduces ischemia/reperfusion injury in rats that correlates with regional angiogenesis and cellular expression of neurotrophin. Stroke. 34:2003;240-241.
15. Ding Y., Li J., Rafols J.A., Phillis J.W., Diaz F.G. Prereperfusion saline infusion into ischemic territory reduces inflammatory injury after transient middle cerebral artery occlusion in rats. Stroke. 33:2002;2492-2498.
16. Ding Y., Yao B., Zhou Y., Park H., McAllister J.P.I.I., Diaz F.G. Pre-reperfusion flushing of ischemic territory a therapeutic study in which histological and behavioral assessments were used to measure ischemia-reperfusion injury in rats with stroke . J Neurosurg. 96:2002;310-319.
17. Heddings A.A., Friel K.M., Plautz E.J., Barbay S., Nudo R.J. Factors contributing to motor impairment and recovery after stroke. Neurorehabil Neural Repair. 14:2000;301-310.
18. Huang J., Kim L.J., Poisik A., Pinsky D.J., Connolly E.S. Jr. Titration of postischemic cerebral hypoperfusion by variation of ischemic severity in a murine model of stroke. Neurosurgery. 45:1999;328-333.
19. Huang Z., Huang P.L., Panahian N., Dalkara T., Fishman M.C., Moskowitz M.A. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science. 265:1994;1883-1885.
20. Isaacs K.R., Anderson B.J., Alcantara A.A., Black J.E., Greenough W.T. Exercise and the brain angiogenesis in the adult rat cerebellum after vigorous physical activity and motor skill learning . J Cereb Blood Flow Metab. 12:1992;110-119.
21. Jenkins W.M., Merzenich M.M. Reorganization of neocortical representations after brain injury a neurophysiological model of the bases of recovery from stroke . Prog Brain Res. 71:1987;249-266.
22. Johansson B.B. Functional outcome in rats transferred to an enriched environment 15 days after focal brain ischemia. Stroke. 27:1996;324-326.
23. Johansson B.B. Brain plasticity and stroke rehabilitation the Willis lecture . Stroke. 31:2000;223-230.
24. Johansson B.B., Grabowski M. Functional recovery after brain infarction plasticity and neural transplantation . Brain Pathol. 4:1994;85-95.
25. Johansson B.B., Ohlsson A.L. Environment, social interaction, and physical activity as determinants of functional outcome after cerebral infarction in the rat. Exp Neurol. 139:1996;322-327.
26. Johansson B.B., Zhao L., Mattsson B. Environmental influence on gene expression and recovery from cerebral ischemia. Acta Neurochir Suppl (Wien). 73:1999;51-55.
27. Jones T.A., Chu C.J., Grande L.A., Gregory A.D. Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J Neurosci. 19:1999;10153-10163.
28. Jones T.A., Hawrylak N., Klintsova A.Y., Greenough W.T. Brain damage, behavior, rehabilitation, rRecovery, and brain plasticity. Ment Retard Dev Disabil Res Rev. 4:1998;231-237.
29. Jones T.A., Kleim J.A., Greenough W.T. Synaptogenesis and dendritic growth in the cortex opposite unilateral sensorimotor cortex damage in adult rats a quantitative electron microscopic examination . Brain Res. 733:1996;142-148.
30. Jones T.A., Schallert T. Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage. Brain Res. 581:1992;156-160.
31. Jones T.A., Schallert T. Use-dependent growth of pyramidal neurons after neocortical damage. J Neurosci. 14:1994;2140-2152.
32. Kleim J.A., Cooper N.R., VandenBerg P.M. Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res. 934:2002;1-6.
33. Kleim J.A., Lussnig E., Schwarz E.R., Comery T.A., Greenough W.T. Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J Neurosci. 16:1996;4529-4535.
34. Klintsova A.Y., Cowell R.M., Swain R.A., Napper R.M., Goodlett C.R., Greenough W.T. Therapeutic effects of complex motor training on motor performance deficits induced by neonatal binge-like alcohol exposure in rats I . Behavioral results. Brain Res. 800:1998;48-61.
35. Klintsova A.Y., Greenough W.T. Synaptic plasticity in cortical systems. Curr Opin Neurobiol. 9:1999;203-208.
36. Koizumi, J, Nakazawa, T (1985) Reperfusable brain infarction model in rat (abstract). Proceedings of the 10th Meeting of the Japanese Stoke Society.
37. Kolb B (1995a) Brain plasticity and recovery of function in adulthood. In: Brain Plasticity and behavior, pp 95-112. Mahwah, New Jersey: Lawrence Erlbaum Associates.
38. Kolb B (1995b) Some basic concepts, examples and biases. In: Brain plasticity and behavior, pp 3-15. Mahwah, New Jersey: Lawrence Erlbaum Associates.
39. Kolb B., Gibb R. Environmental enrichment and cortical injury behavioral and anatomical consequences of frontal cortex lesions . Cereb Cortex. 1:1991;189-198.
40. Li Y., Jiang N., Powers C., Chopp M. Neuronal damage and plasticity identified by microtubule-associated protein 2, growth-associated protein 43, and cyclin D1 immunoreactivity after focal cerebral ischemia in rats. Stroke. 29:1998;1972-1980.
41. Markgraf C.G., Green E.J., Hurwitz B.E., Morikawa E., Dietrich W.D., McCabe P.M., Ginsberg M.D., Schneiderman N. Sensorimotor and cognitive consequences of middle cerebral artery occlusion in rats. Brain Res. 575:1992;238-246.
42. Meyer L.S., Kotch L.E., Riley E.P. Neonatal ethanol exposure functional alterations associated with cerebellar growth retardation . Neurotoxicol Teratol. 12:1990;15-22.
43. Niimura K., Chugani D.C., Muzik O., Chugani H.T. Cerebellar reorganization following cortical injury in humans effects of lesion size and age . Neurology. 52:1999;792-797.
44. Nudo R.J. Remodeling of cortical motor representations after stroke implications for recovery from brain damage . Mol Psychiatry. 2:1997;188-191.
45. Nudo R.J. Recovery after damage to motor cortical areas. Curr Opin Neurobiol. 9:1999;740-747.
46. Nudo R.J., Milliken G.W. Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J Neurophysiol. 75:1996;2144-2149.
47. Nudo R.J., Plautz E.J., Frost S.B. Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle Nerve. 24:2001;1000-1019.
48. Nudo R.J., Wise B.M., SiFuentes F., Milliken G.W. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science. 272:1996;1791-1794.
49. Ohlsson A.L., Johansson B.B. Environment influences functional outcome of cerebral infarction in rats. Stroke. 26:1995;644-649.
50. Okada M., Tamura A., Urae A., Nakagomi T., Kirino T., Mine K., Fujiwara M. Long-term spatial cognitive impairment following middle cerebral artery occlusion in rats a behavioral study . J Cereb Blood Flow Metab. 15:1995;505-512.
51. Pons T.P., Garraghty P.E., Mishkin M. Lesion-induced plasticity in the second somatosensory cortex of adult macaques. Proc Natl Acad Sci USA. 85:1988;5279-5281.
52. Pulsinelli W., Jacewicz M. Animal models of brain ischemia. Barnett H.J.M., Stein B.M., Mohr J.P., Yatsu F.M. Stroke: pathophysiology, diagnosis, and management. 1992;49-67 Churchill Livingstone, New York.
53. Remple M.S., Bruneau R.M., VandenBerg P.M., Goertzen C., Kleim J.A. Sensitivity of cortical movement representations to motor experience evidence that skill learning but not strength training induces cortical reorganization . Behav Brain Res. 123:2001;133-141.
54. Risedal A., Mattsson B., Dahlqvist P., Nordborg C., Olsson T., Johansson B.B. Environmental influences on functional outcome after a cortical infarct in the rat. Brain Res Bull. 58:2002;315-321.
55. Rogers D.C., Campbell C.A., Stretton J.L., Mackay K.B. Correlation between motor impairment and infarct volume after permanent and transient middle cerebral artery occlusion in the rat. Stroke. 28:1997;2060-2065.
56. Rosenzweig M.R. Experience, memory, and the brain. Am Psychol. 39:1984;365-376.
57. Stroemer R.P., Kent T.A., Hulsebosch C.E. Enhanced neocortical neural sprouting, synaptogenesis, and behavioral recovery with D-amphetamine therapy after neocortical infarction in rats. Stroke. 29:1998;2381-2393.
58. Swanson R.A., Morton M.T., Tsao-Wu G., Savalos R.A., Davidson C., Sharp F.R. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab. 10:1990;290-293.
59. Weiller C. Imaging recovery from stroke. Exp Brain Res. 123:1998;13-17.
60. Weiller C., Ramsay S.C., Wise R.J., Friston K.J., Frackowiak R.S. Individual patterns of functional reorganization in the human cerebral cortex after capsular infarction. Ann Neurol. 33:1993;181-189.
61. Winfree C.J., Baker C.J., Connolly E.S., Fiore A.J., Solomon R.A. Mild hypothermia reduces penumbral glutamate levels in the rat permanent focal cerebral ischemia model. Neurosurgery. 38:1996;1216-1222.
62. Witte O.W., Stoll G. Delayed and remote effects of focal cortical infarctions secondary damage and reactive plasticity . Adv Neurol. 73:1997;207-227.
63. Xerri C., Merzenich M.M., Peterson B.E., Jenkins W. Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J Neurophysiol. 79:1998;2119-2148.
64. Yamamoto M., Tamura A., Kirino T., Shimizu M., Sano K. Behavioral changes after focal cerebral ischemia by left middle cerebral artery occlusion in rats. Brain Res. 452:1988;323-328.
65. Yang Y.R., Wang R.Y., Wang P.S. Early and late treadmill training after focal brain ischemia in rats. Neurosci Lett. 339:2003;91-94.
66. Zea Longa Z., Weinstein P.R., Carlson S., Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke. 20:1989;84-91.
67. Zhao L.R., Mattsson B., Johansson B.B. Environmental influence on brain-derived neurotrophic factor messenger RNA expression after middle cerebral artery occlusion in spontaneously hypertensive rats. Neuroscience. 97:2000;177-184.