Motor skill training, but not voluntary exercise, improves skilled reaching after unilateral ischemic lesions of the sensorimotor cortex in rats

Neurorehabilitation and Neural Repair

Volumn 22, Issue 3, 2008, Pages 250-261

  Maldonado, Monica A ^a   Allred, Rachel P ^a   Felthauser, Erik L ^a   Jones, Theresa A ^a,b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b Department of Psychology ^*  (United States)

Author keywords

Exercise; Experience dependent plasticity; Rehabilitation; Skilled reaching

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARM MOVEMENT; ARTICLE; BRAIN ISCHEMIA; CONTROLLED STUDY; EXERCISE; FEMALE; FORELIMB; IMMUNOCYTOCHEMISTRY; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NONHUMAN; RAT; RUNNING; SENSORIMOTOR CORTEX; SKILL;

AGE FACTORS; ANIMALS; BRAIN ISCHEMIA; DISEASE MODELS, ANIMAL; FEMALE; FORELIMB; LEARNING; MOTOR ACTIVITY; MOTOR CORTEX; MOTOR SKILLS; MOVEMENT DISORDERS; MUSCLE, SKELETAL; NEURONAL PLASTICITY; PARESIS; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL THERAPY MODALITIES; RATS; RATS, LONG-EVANS;

EID: 40749159306     PISSN: 15459683     EISSN: 15526844     Source Type: Journal    
DOI: 10.1177/1545968307308551     Document Type: Article

References (71)

1. Kolb B., Gibb R. Environmental enrichment and cortical injury: behavioral and anatomical consequences of frontal cortex lesions. Cereb Cortex. 1991 ; 1 (2). 189-198.
2. Will B., Galani R., Kelche C., Rosenzweig MR Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog Neurobiol. 2004 ; 72 (3). 167-182.
3. Vaynman S., Gomez-Pinilla F. License to run: exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabil Neural Repair. 2005 ; 19 (4). 283-295.
4. Ding Q., et al. Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience. 2006 ; 140 (3). 823-833.
5. Griesbach GS, Hovda DA, Molteni R., Wu A., Gómez-Pinilla F. Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience. 2004 ; 125 (1). 129-139.
6. Molteni R., Zheng J. -Q, Ying Z., Gómez-Pinilla F., Twiss JL Voluntary exercise increases axonal regeneration from sensory neurons. Proc Natl Acad Sci U S A. 2004 ; 101 (22). 8473-8478.
7. Ying Z., Roy RR, Edgerton VR, Gómez-Pinilla F. Exercise restores levels of neurotrophins and synaptic plasticity following spinal cord injury. Exp Neurol. 2005 ; 193 (2). 411-419.
8. Hutchinson, KJ, Gómez-Pinilla F., Crowe MJ, Ying Z., Basso DM Three exercise paradigms differentially improve sensory recovery after spinal cord contusion in rats. Brain. 2004 ; 127 (Pt 6). 1403-1414.
9. Wang RY, Yang YR, Yu SM Protective effects of treadmill training on infarction in rats. Brain Res. 2001 ; 922 (1). 140-143.
10. Adkins DL, Boychuk A., Remple MS, Kleim JA Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J Appl Physiol. 2006 ; 101 (6). 1776-1782.
11. Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci U S A. 1990 ; 87 (14). 5568-5572.
12. Monfils MH, Plautz EJ, Kleim JA In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience. Neuroscientist. 2005 ; 11 (5). 471-483.
13. Kleim JA, Barbay S., Nudo RJ Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol. 1998 ; 80 (6). 3321-3325.
14. Markham JA, Greenough WT Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biol. 2004 ; 1 (4). 351-363.
15. Nudo RJ, Milliken GW Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J Neurophysiol. 1996 ; 75 (5). 2144-2149.
16. Conner JM, Chiba AA, Tuszynski MH The basal forebrain cholinergic system is essential for cortical plasticity and functional recovery following brain injury. Neuron. 2005 ; 46 (2). 173-179.
17. Ramanathan D., Conner JM, Tuszynski MH A form of motor cortical plasticity that correlates with recovery of function after brain injury. Proc Natl Acad Sci U S A. 2006 ; 103 (30). 11370-11375.
18. Biernaskie J., Corbett D. Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci. 2001 ; 21 (14). 5272-5280.
19. DeBow SB, Davies MLA, 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 (4). 1021-1026.
20. Gharbawie OA, Gonzalez CL, Whishaw IQ 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. 2005 ; 156 (1). 125-137.
21. Vaynman S., Ying Z., Gomez-Pinilla F. Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience. 2003 ; 122 (3). 647-657.
22. Allred RP, Jones TA Unilateral ischemic sensorimotor cortical damage in female rats: forelimb behavioral effects and dendritic structural plasticity in the contralateral homotopic cortex. Exp Neurol. 2004 ; 190 (2). 433-445.
23. Woolley CS, McEwen BS Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol. 1993 ; 336 (2). 293-306.
24. Chen J., Chopp M. Li, Y. Neuroprotective effects of progesterone after transient middle cerebral artery occlusion in rat. J Neurol Sci. 1999 ; 171 (1). 24-30.
25. Tropp J., Markus EJ Effects of mild food deprivation on the estrous cycle of rats. Physiol Behav. 2001 ; 73 (4). 553-559.
26. Adkins DL, Voorhies AC, Jones TA Behavioral and neuroplastic effects of focal endothelin-1 induced sensorimotor cortex lesions. Neuroscience. 2004 ; 128 (3). 473-486.
27. 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 (11). 2623-2629.
28. Peterson GM, McGiboney DR Jr. Reeducation of handedness in the rat following cerebral injuries. J Comp Physiol Psychol. 1951 ; 44 (2). 191-196.
29. Whishaw IQ Lateralization and reaching skill related: results and implications from a large sample of Long-Evans rats. Behav Brain Res. 1992 ; 52 (1). 45-48.
30. Bury SD, Jones TA Unilateral sensorimotor cortex lesions in adult rats facilitate motor skill learning with the "unaffected" forelimb and training-induced dendritic structural plasticity in the motor cortex. J Neurosci. 2002 ; 22 (19). 8597-8606.
31. Hsu JE, Jones TA Contralesional neural plasticity and functional changes in the less-affected forelimb after large and small cortical infarcts in rats. Exp Neurol. 2006 ; 201 (2). 479-494.
32. Kozlowski DA, James DC, Schallert T. Use-dependent exaggeration of neuronal injury after unilateral sensorimotor cortex lesions. J Neurosci. 1996 ; 16 (15). 4776-4786.
33. Whishaw IQ, O'Connor WT, Dunnett SB The contributions of motor cortex, nigrostriatal dopamine and caudate-putamen to skilled forelimb use in the rat. Brain. 1986 ; 109 (Pt 5). 805-843.
34. Barth TM, Jones TA, Schallert T. Functional subdivisions of the rat somatic sensorimotor cortex. Behav Brain Res. 1990 ; 39 (1). 73-95.
35. Jones TA Multiple synapse formation in the motor cortex opposite unilateral sensorimotor cortex lesions in adult rats. J Comp Neurol. 1999 ; 414 (1). 57-66.
36. Schmanke TD, Avery RA, Barth TM The effects of amphetamine on recovery of function after cortical damage in the rat depend on the behavioral requirements of the task. J Neurotrauma. 1996 ; 13 (6). 293-307.
37. Gundersen HJ, Bendtsen TF, Korbo L., et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis. 1988 ; 96 (5). 379-394.
38. Paxinos CWG. The Rat Brain in Stereotaxic Coordinates. 2 nd ed. Sydney: Academic Press ; 1986.
39. Woodlee MT, Schallert T. The interplay between behavior and neurodegeneration in rat models of Parkinson's disease and stroke. Restor Neurol Neurosci. 2004 ; 22 (3-5). 153-161.
40. West MJ, Slomianka L., Gundersen HJ Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec. 1991 ; 231 (4). 482-497.
41. Dancause N., Barbay S., Frost SB, et al. Extensive cortical rewiring after brain injury. J Neurosci. 2005 ; 25 (44). 10167-10179.
42. Friel KM, Nudo RJ Recovery of motor function after focal cortical injury in primates: compensatory movement patterns used during rehabilitative training. Somatosens Mot Res. 1998 ; 15 (3). 173-189.
43. Friel KM, Barbay S., Frost SB, et al. Effects of a rostral motor cortex lesion on primary motor cortex hand representation topography in primates. Neurorehabil Neural Repair. 2007 ; 21 (1). 51-61.
44. Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci. 1996 ; 16 (2). 785-807.
45. Komitova M., Zhao LR, Gidö G., Johansson BB, Eriksson P. Postischemic exercise attenuates whereas enriched environment has certain enhancing effects on lesion-induced subventricular zone activation in the adult rat. Eur J Neurosci. 2005 ; 21 (9). 2397-2405.
46. Johansson BB, Ohlsson AL Environment, social interaction, and physical activity as determinants of functional outcome after cerebral infarction in the rat. Exp Neurol. 1996 ; 139 (2). 322-327.
47. Ding YH, Li J., Zhou Y., Rafols JA, Clark JC, Ding Y. Cerebral angiogenesis and expression of angiogenic factors in aging rats after exercise. Curr Neurovasc Res. 2006 ; 3 (1). 15-23.
48. Ding YH, Xia-Dong L., Jie L., et al. Exercise-induced overexpression of angiogenic factors and reduction of ischemia/reperfusion injury in stroke. Curr Neurovasc Res. 2004 ; 1 (5). 411-420.
49. Vaynman S., Ying Z., Gomez-Pinilla F. Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci. 2004 ; 20 (10). 2580-2590.
50. Kleim JA, Cooper NR, VandenBerg PM Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res. 2002 ; 934 (1). 1-6.
51. Swain RA, Harris AB, Wiener EC, et al. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience. 2003 ; 117 (4). 1037-1046.
52. Adkins DL, Jones TA D-amphetamine enhances skilled reaching after ischemic cortical lesions in rats. Neurosci Lett. 2005 ; 380 (3). 214-218.
53. Adkins-Muir DL, Jones TA Cortical electrical stimulation combined with rehabilitative training: enhanced functional recovery and dendritic plasticity following focal cortical ischemia in rats. Neurol Res. 2003 ; 25 (8). 780-788.
54. Adlard PA, Perreau VM, Engesser-Cesar C., Cotman CW The timecourse of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neurosci Lett. 2004 ; 363 (1). 43-48.
55. Klintsova AY, Dickson E., Yoshida R., Greenough WT Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res. 2004 ; 1028 (1). 92-104.
56. Griesbach GS, Gomez-Pinilla F., Hovda DA The upregulation of plasticity-related proteins following TBI is disrupted with acute voluntary exercise. Brain Res. 2004 ; 1016 (2). 154-162.
57. Ploughman M., Granter-Button S., Chernenko G., Tucker BA, Mearow KM, Corbett D. Endurance exercise regimens induce differential effects on brain-derived neurotrophic factor, synapsin-I and insulin-like growth factor I after focal ischemia. Neuroscience. 2005 ; 136 (4). 991-1001.
58. Mattson MP, Wan R. Beneficial effects of intermittent fasting and caloric restriction on the cardiovascular and cerebrovascular systems. J Nutr Biochem. 2005 ; 16 (3). 129-137.
59. Mattson MP Energy intake, meal frequency, and health: a neuro-biological perspective. Annu Rev Nutr. 2005 ; 25: 237-260.
60. Allen PB, Ouimet CC, Greengard P. Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci U S A. 1997 ; 94 (18). 9956-9961.
61. Feng J., Yan Z., Ferreira A., et al. Spinophilin regulates the formation and function of dendritic spines. Proc Natl Acad Sci U S A. 2000 ; 97 (16). 9287-9292.
62. Kosar E., Grill HJ, Norgren R. Gustatory cortex in the rat. I. Physiological properties and cytoarchitecture. Brain Res. 1986 ; 379 (2). 329-341.
63. Griesbach GS, Gomez-Pinilla F., Hovda DA Time window for voluntary exercise-induced increases in hippocampal neuroplasticity molecules after traumatic brain injury is severity dependent. J Neurotrauma. 2007 ; 24 (7). 1161-1171.
64. Ploughman M., Granter-Button S., Chernenko G., et al. Exercise intensity influences the temporal profile of growth factors involved in neuronal plasticity following focal ischemia. Brain Res. 2007 ; 1150: 207-216.
65. Leasure JL, Schallert T. Consequences of forced disuse of the impaired forelimb after unilateral cortical injury. Behav Brain Res. 2004 ; 150 (1-2). 83-91.
66. 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 (2). 286-292.
67. Biernaskie J., Chernenko G., Corbett D. Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. J Neurosci. 2004 ; 24 (5). 1245-1254.
68. Barbay S., Plautz EJ, Friel KM, et al. Behavioral and neurophysiological effects of delayed training following a small ischemic infarct in primary motor cortex of squirrel monkeys. Exp Brain Res. 2006 ; 169 (1). 106-116.
69. Li J., Luan X., Clark JC, Rafols JA, Ding Y. Neuroprotection against transient cerebral ischemia by exercise pre-conditioning in rats. Neurol Res. 2004 ; 26 (4). 404-408.
70. Stein DG Brain damage, sex hormones and recovery: a new role for progesterone and estrogen ? Trends Neurosci. 2001 ; 24 (7). 386-391.
71. Kleim JA, Jones TA, Schallert T. Motor enrichment and the induction of plasticity before or after brain injury. Neurochem Res. 2003 ; 28 (11). 1757-1769.