Combining Multiple Types of Motor Rehabilitation Enhances Skilled Forelimb Use Following Experimental Traumatic Brain Injury in Rats

Neurorehabilitation and Neural Repair

Volumn 29, Issue 10, 2015, Pages 989-1000

  Adkins, Deanna L ^a   Ferguson, Lindsay ^b   Lance, Steven ^b   Pevtsov, Aleksandr ^b   McDonough, Kevin ^b   Stamschror, Justin ^b   Jones, Theresa A ^c   Kozlowski, Dorothy A ^b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b DEPAUL UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

constraint induced movement therapy; controlled cortical impact; exercise; motor rehabilitation; neuroplasticity; recovery of function

Indexed keywords

AEROBIC EXERCISE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; FORELIMB; INJURY SEVERITY; MALE; MOTOR COORDINATION; MOTOR PERFORMANCE; NEUROPROTECTION; NONHUMAN; RAT; TRAUMATIC BRAIN INJURY; ANALYSIS OF VARIANCE; ANIMAL; BRAIN INJURIES; COMPLICATION; CONVALESCENCE; DISEASE MODEL; FEEDING BEHAVIOR; HEMISPHERIC DOMINANCE; LONG EVANS RAT; MOTOR SKILLS DISORDERS; PATHOLOGY; PHYSIOLOGY; PHYSIOTHERAPY; RANDOMIZED CONTROLLED TRIAL; TIME FACTOR; UPPER LIMB;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN INJURIES; DISEASE MODELS, ANIMAL; FEEDING BEHAVIOR; FUNCTIONAL LATERALITY; MALE; MOTOR SKILLS DISORDERS; PHYSICAL CONDITIONING, ANIMAL; PHYSICAL THERAPY MODALITIES; RATS; RATS, LONG-EVANS; RECOVERY OF FUNCTION; TIME FACTORS; UPPER EXTREMITY;

EID: 84945121200     PISSN: 15459683     EISSN: 15526844     Source Type: Journal    
DOI: 10.1177/1545968315576577     Document Type: Article

References (63)

1. Faul M, Xu L, Wald MM, Coronado VG,. Traumatic Brain Injury in the United States: Emergency Department Visits, Hospitalizations and Deaths 2002-2006. Atlanta, GA: Centers for Disease Control and Prevention; 2010.
2. Krauss JK, Jankovic J,. Movement disorders after TBI. In: Zasler ND, Katz DI, Zafonte RD, eds. Brain Injury Medicine: Principles and Practice. New York, NY: Demos; 2007: 469-489.
3. Walker WC, Pickett TC,. Motor impairment after severe traumatic brain injury: a longitudinal multicenter study. J Rehabil Res Dev. 2007; 44: 975-982.
4. Kozlowski DA, Leasure JL, Schallert T,. The control of movement following traumatic brain injury. Compr Physiol. 2013; 3: 121-139.
5. Weightman MM, Bolgla R, McCulloch KL, Peterson MD,. Physical therapy recommendations for service members with mild traumatic brain injury. J Head Trauma Rehabil. 2010; 25: 206-218.
6. Greenwald BD, Rigg JL,. Neurorehabilitation in traumatic brain injury: does it make a difference? Mt Sinai J Med. 2009; 76: 182-189.
7. Dimyan MA, Cohen LG,. Neuroplasticity in the context of motor rehabilitation after stroke. Nat Rev Neurol. 2011; 7: 76-85.
8. Dobkin BH,. Neurobiology of rehabilitation. Ann N Y Acad Sci. 2004; 1038: 148-170.
9. Johansson BB,. Brain plasticity and stroke rehabilitation: the Willis lecture. Stroke. 2000; 31: 223-230.
10. Veerbeek JM, van Wegen E, van Peppen R, et al. What is the evidence for physical therapy poststroke? A systematic review and meta-analysis. PLoS One. 2014; 9: e87987.
11. McIntyre A, Viana R, Janzen S, Mehta S, Pereira S, Teasell R,. Systematic review and meta-analysis of constraint-induced movement therapy in the hemiparetic upper extremity more than six months post stroke. Top Stroke Rehabil. 2012; 19: 499-513.
12. Wolf SL, Winstein CJ, Miller JP, et al. Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. JAMA. 2006; 296: 2095-2104.
13. Fritz SL, Butts RJ, Wolf SL,. Constraint-induced movement therapy: from history to plasticity. Expert Rev Neurother. 2012; 12: 191-198.
14. Gauthier LV, Taub E, Perkins C, Ortmann M, Mark VW, Uswatte G,. Remodeling the brain: plastic structural brain changes produced by different motor therapies after stroke. Stroke. 2008; 39: 1520-1525.
15. Wise EK, Hoffman JM, Powell JM, Bombardier CH, Bell KR,. Benefits of exercise maintenance after traumatic brain injury. Arch Phys Med Rehabil. 2012; 93: 1319-1323.
16. Brazzelli M, Saunders DH, Greig CA, Mead GE,. Physical fitness training for stroke patients. Cochrane Database Syst Rev. 2011;(11): CD003316.
17. Jones TA, Adkins DL,. Behavioral influences on neuronal events after stroke, section I. In: Cramer SC, Nudo RJ, eds. Brain Repair After Stroke. Cambridge, UK: Cambridge University Press; 2010:chap 3.
18. Kleim JA, Jones TA,. Principles of experience-dependent neural plasticity: implications for rehabilitation after brain damage. J Speech Lang Hear Res. 2008; 51: S225-S239.
19. 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.
20. Nudo RJ, Wise BM, SiFuentes F, Milliken GW,. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science. 1996; 272: 1791-1794.
21. Castro-Alamancos MA, Borrel J,. Functional recovery of forelimb response capacity after forelimb primary motor cortex damage in the rat is due to the reorganization of adjacent areas of cortex. Neuroscience. 1995; 68: 793-805.
22. Tennant KA, Kerr AL, Adkins DL, et al. Age-dependent reorganization of peri-infarct "premotor" cortex with task-specific rehabilitative training in mice. Neurorehabil Neural Repair. 2015; 29: 193-202.
23. 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: 173-179.
24. Lam TI, Bingham D, Chang TJ, et al. Beneficial effects of minocycline and botulinum toxin-induced constraint physical therapy following experimental traumatic brain injury. Neurorehabil Neural Repair. 2013; 27: 889-899.
25. Voss MW, Vivar C, Kramer AF, van Praag H,. Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn Sci. 2013; 17: 525-544.
26. 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: 1037-1046.
27. Adkins DL, Boychuk J, Remple MS, Kleim JA,. Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J Appl Physiol. 2006; 101: 1776-1782.
28. Austin MW, Ploughman M, Glynn L, Corbett D,. Aerobic exercise effects on neuroprotection and brain repair following stroke: a systematic review and perspective. Neurosci Res. 2014; 87: 8-15.
29. Griesbach GS,. Exercise after traumatic brain injury: is it a double-edged sword? PM R. 2011; 3 (6, suppl 1): S64-S72.
30. 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: 1161-1171.
31. Hicks RR, Martin VB, Zhang L, Seroogy KB,. Mild experimental brain injury differentially alters the expression of neurotrophic and neurotrophin receptor mRNAs in the hippocampus. Exp Neurol. 1999; 160: 469-478.
32. Li HH, Lee SM, Cai Y, Sutton RL, Hovda DA,. Differential gene expression in hippocampus following experimental brain trauma reveals distinct features of moderate and severe injuries. J Neurotrauma. 2004; 21: 1141-1153.
33. Thompson SN, Gibson TR, Thompson BM, Deng Y, Hall ED,. Relationship of calpain-mediated proteolysis to the expression of axonal and synaptic plasticity markers following traumatic brain injury in mice. Exp Neurol. 2006; 201: 253-265.
34. Jones TA, Liput DJ, Maresh EL, et al. Use-dependent dendritic regrowth is limited after unilateral controlled cortical impact to the forelimb sensorimotor cortex. J Neurotrauma. 2012; 29: 1455-1468.
35. Adkins DL, Voorhies AC, Jones TA,. Behavioral and neuroplastic effects of focal endothelin-1 induced sensorimotor cortex lesions. Neuroscience. 2004; 128: 473-486.
36. Jones TA, Schallert T,. Use-dependent growth of pyramidal neurons after neocortical damage. J Neurosci. 1994; 14: 2140-2152.
37. Adams FS, Schwarting RK, Huston JP,. Behavioral and neurochemical asymmetries following unilateral trephination of the rat skull: is this control operation always appropriate? Physiol Behav. 1994; 55: 947-952.
38. Miklyaeva EI, Castaneda E, Whishaw IQ,. Skilled reaching deficits in unilateral dopamine-depleted rats: impairments in movement and posture and compensatory adjustments. J Neurosci. 1994; 14 (11, pt 2): 7148-7158.
39. Klein A, Sacrey LA, Whishaw IQ, Dunnett SB,. The use of rodent skilled reaching as a translational model for investigating brain damage and disease. Neurosci Biobehav Rev. 2012; 36: 1030-1042.
40. 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.
41. Alaverdashvili M, Leblond H, Rossignol S, Whishaw IQ,. Cineradiographic (video X-ray) analysis of skilled reaching in a single pellet reaching task provides insight into relative contribution of body, head, oral, and forelimb movement in rats. Behav Brain Res. 2008; 192: 232-247.
42. Hernandez TD, Schallert T,. Seizures and recovery from experimental brain damage. Exp Neurol. 1988; 102: 318-324.
43. Kozlowski DA, James DC, Schallert T,. Use-dependent exaggeration of neuronal injury after unilateral sensorimotor cortex lesions. J Neurosci. 1996; 16: 4776-4786.
44. Hsu JE, Jones TA,. Time-sensitive enhancement of motor learning with the less-affected forelimb after unilateral sensorimotor cortex lesions in rats. Eur J Neurosci. 2005; 22: 2069-2080.
45. Soblosky JS, Matthews MA, Davidson JF, Tabor SL, Carey ME,. Traumatic brain injury of the forelimb and hindlimb sensorimotor areas in the rat: physiological, histological and behavioral correlates. Behav Brain Res. 1996; 79: 79-92.
46. Nishibe M, Barbay S, Guggenmos D, Nudo RJ,. Reorganization of motor cortex after controlled cortical impact in rats and implications for functional recovery. J Neurotrauma. 2010; 27: 2221-2232.
47. Griesbach GS, Hovda DA, Molteni R, Wu A, Gomez-Pinilla F,. Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience. 2004; 125: 129-139.
48. Hicks RR, Boggs A, Leider D, et al. Effects of exercise following lateral fluid percussion brain injury in rats. Restor Neurol Neurosci. 1998; 12: 41-47.
49. Griesbach GS, Hovda DA, Gomez-Pinilla F, Sutton RL,. Voluntary exercise or amphetamine treatment, but not the combination, increases hippocampal brain-derived neurotrophic factor and synapsin I following cortical contusion injury in rats. Neuroscience. 2008; 154: 530-540.
50. Kline AE, Olsen AS, Sozda CN, Hoffman AN, Cheng JP,. Evaluation of a combined treatment paradigm consisting of environmental enrichment and the 5-HT(1A) receptor agonist buspirone after experimental traumatic brain injury. J Neurotrauma. 2012; 29: 1960-1969.
51. 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.
52. Crane AT, Fink KD, Smith JS,. The effects of acute voluntary wheel running on recovery of function following medial frontal cortical contusions in rats. Restor Neurol Neurosci. 2012; 30: 325-333.
53. Shaw SE, Morris DM, Uswatte G, McKay S, Meythaler JM, Taub E,. Constraint-induced movement therapy for recovery of upper-limb function following traumatic brain injury. J Rehabil Res Dev. 2005; 42: 769-778.
54. Joo HW, Hyun JK, Kim TU, Chae SH, Lee YI, Lee SJ,. Influence of constraint-induced movement therapy upon evoked potentials in rats with cerebral infarction. Eur J Neurosci. 2012; 36: 3691-3697.
55. Maier IC, Baumann K, Thallmair M, Weinmann O, Scholl J, Schwab ME,. Constraint-induced movement therapy in the adult rat after unilateral corticospinal tract injury. J Neurosci. 2008; 28: 9386-9403.
56. Allred RP, Jones TA,. Maladaptive effects of learning with the less-affected forelimb after focal cortical infarcts in rats. Exp Neurol. 2008; 210: 172-181.
57. Dromerick AW, Lang CE, Birkenmeier RL, et al. Very early constraint-induced movement during stroke rehabilitation (VECTORS): a single-center RCT. Neurology. 2009; 73: 195-201.
58. Nishibe M, Urban ET III, Barbay S, Nudo RJ,. Rehabilitative training promotes rapid motor recovery but delayed motor map reorganization in a rat cortical ischemic infarct model [published online July 22, 2014]. Neurorehabil Neural Repair. doi: 10.1177/1545968314543499.
59. Jones TA, Allred RP, Adkins DL, Hsu JE, O'Bryant A, Maldonado MA,. Remodeling the brain with behavioral experience after stroke. Stroke. 2009; 40 (3, suppl): S136-S138.
60. Sampaio-Baptista C, Khrapitchev AA, Foxley S, et al. Motor skill learning induces changes in white matter microstructure and myelination. J Neurosci. 2013; 33: 19499-19503.
61. Hotting K, Roder B,. Beneficial effects of physical exercise on neuroplasticity and cognition. Neurosci Biobehav Rev. 2013; 37 (9, pt B): 2243-2257.
62. Cole JT, Yarnell A, Kean WS, et al. Craniotomy: true sham for traumatic brain injury, or a sham of a sham? J Neurotrauma. 2011; 28: 359-369.
63. Belke TW,. Postreinforcement pause duration varies within a session and with a variable response requirement but not as a function of prior revolutions. Psychol Rec. 2011; 61: 213-226.