Effects of rehabilitative training on recovery of hand motor function: A review of animal studies

Neuroscience Research

Volumn 78, Issue 1, 2014, Pages 9-15

  Higo, Noriyuki ^a  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

Brain damage; Corticospinal tract; Hand movements; Macaque monkey; Manual dexterity; Spinal cord damage

Indexed keywords

BRAIN INJURY; CONVALESCENCE; EXPERIMENTAL ANIMAL; FUNCTIONAL NEUROIMAGING; FUNCTIONAL TRAINING; GENE EXPRESSION ASSAY; HAND FUNCTION; MACACA; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NONHUMAN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PYRAMIDAL TRACT; REVIEW; SPINAL CORD INJURY; TREATMENT OUTCOME; ANIMAL; BRAIN INJURIES; CERVICAL SPINE; HAND; MOTOR CORTEX; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; RHESUS MONKEY; SPINAL CORD INJURIES; BODY MOVEMENT; CLINICAL OBSERVATION; GENE EXPRESSION; HAND MOVEMENT; HUMAN; MUSCLE TRAINING; PRECISION GRIP; SENSORIMOTOR CORTEX; SPINAL CORD LESION; STROKE PATIENT;

ANIMALS; BRAIN INJURIES; CERVICAL VERTEBRAE; HAND; MACACA MULATTA; MOTOR CORTEX; MOTOR SKILLS; PYRAMIDAL TRACTS; RATS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84892673729     PISSN: 01680102     EISSN: 18728111     Source Type: Journal    
DOI: 10.1016/j.neures.2013.09.008     Document Type: Review

References (53)

1. Alstermark B., Ogawa J., Isa T. Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurons and polysynaptic EPSPs via segmental interneurons. J. Neurophysiol. 2004, 91:1832-1839.
2. Barbas H., Pandya D.N. Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. J. Comp. Neurol. 1987, 256:211-228.
3. Barbay S., Guggenmos D.J., Nishibe M., Nudo R.J. Motor representations in the intact hemisphere of the rat are reduced after repetitive training of the impaired forelimb. Neurorehabil. Neural Repair 2013, 27:381-384.
4. Barbay S., Plautz E.J., Friel K.M., Frost S.B., Dancause N., Stowe A.M., Nudo R.J. Behavioral and neurophysiological effects of delayed training following a small ischemic infarct in primary motor cortex of squirrel monkeys. Exp. Brain Res. 2006, 169:106-116.
5. Benowitz L.I., Routtenberg A. A membrane phosphoprotein associated with neural development, axonal regeneration, phospholipid metabolism, and synaptic plasticity. Trends Neurosci. 1987, 10:527-532.
6. Benowitz L.I., Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci. 1997, 20:84-91.
7. Biernaskie J., Chernenko G., Corbett D. Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. J. Neurosci. 2004, 24:1245-1254.
8. Biernaskie J., Corbett D. Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J. Neurosci. 2001, 21:5272-5280.
9. Carmichael S.T., Wei L., Rovainen C.M., Woolsey T.A. New patterns of intracortical projections after focal cortical stroke. Neurobiol. Dis. 2001, 8:910-922.
10. Choi D.W., Koh J.Y., Peters S. Pharmacology of glutamate neurotoxicity in cortical cell culture: attenuation by NMDA antagonists. J. Neurosci. 1988, 8:185-196.
11. Choi D.W., Maulucci-Gedde M., Kriegstein A.R. Glutamate neurotoxicity in cortical cell culture. J. Neurosci. 1987, 7:357-368.
12. Coupar F., Pollock A., Rowe P., Weir C., Langhorne P. Predictors of upper limb recovery after stroke: a systematic review and meta-analysis. Clin. Rehabil. 2012, 26:291-313.
13. Courtine G., Bunge M.B., Fawcett J.W., Grossman R.G., Kaas J.H., Lemon R., Maier I., Martin J., Nudo R.J., Ramon-Cueto A., Rouiller E.M., Schnell L., Wannier T., Schwab M.E., Edgerton V.R. Can experiments in nonhuman primates expedite the translation of treatments for spinal cord injury in humansα. Nat. Med. 2007, 13:561-566.
14. Courtine G., Roy R.R., Raven J., Hodgson J., McKay H., Yang H., Zhong H., Tuszynski M.H., Edgerton V.R. Performance of locomotion and foot grasping following a unilateral thoracic corticospinal tract lesion in monkeys (Macaca mulatta). Brain 2005, 128:2338-2358.
15. Dancause N., Barbay S., Frost S.B., Plautz E.J., Chen D., Zoubina E.V., Stowe A.M., Nudo R.J. Extensive cortical rewiring after brain injury. J. Neurosci. 2005, 25:10167-10179.
16. Denny J.B. Molecular mechanisms, biological actions, and neuropharmacology of the growth-associated protein GAP-43. Curr. Neuropharmacol. 2006, 4:293-304.
17. Freund P., Schmidlin E., Wannier T., Bloch J., Mir A., Schwab M.E., Rouiller E.M. Nogo-A-specific antibody treatment enhances sprouting and functional recovery after cervical lesion in adult primates. Nat. Med. 2006, 12:790-792.
18. Frost S.B., Barbay S., Friel K.M., Plautz E.J., Nudo R.J. Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J. Neurophysiol. 2003, 89:3205-3214.
19. Girgis J., Merrett D., Kirkland S., Metz G.A., Verge V., Fouad K. Reaching training in rats with spinal cord injury promotes plasticity and task specific recovery. Brain 2007, 130:2993-3003.
20. Higo N., Nishimura Y., Murata Y., Oishi T., Yoshino-Saito K., Takahashi M., Tsuboi F., Isa T. Increased expression of the growth-associated protein 43 gene in the sensorimotor cortex of the macaque monkey after lesioning the lateral corticospinal tract. J. Comp. Neurol. 2009, 516:493-506.
21. Higo N., Oishi T., Yamashita A., Matsuda K., Hayashi M. Expression of GAP-43 and SCG10 mRNAs in lateral geniculate nucleus of normal and monocularly deprived macaque monkeys. J. Neurosci. 2000, 20:6030-6038.
22. Higo N., Sato A., Yamamoto T., Nishimura Y., Oishi T., Murata Y., Onoe H., Yoshino-Saito K., Tsuboi F., Takahashi M., Isa T., Kojima T. SPP1 is expressed in corticospinal neurons of the macaque sensorimotor cortex. J. Comp. Neurol. 2010, 518:2633-2644.
23. Humm J.L., Kozlowski D.A., Bland S.T., James D.C., Schallert T. Use-dependent exaggeration of brain injury: is glutamate involvedα. Exp. Neurol. 1999, 157:349-358.
24. Isa T., Ohki Y., Alstermark B., Pettersson L.G., Sasaki S. Direct and indirect cortico-motoneuronal pathways and control of hand/arm movements. Physiology (Bethesda) 2007, 22:145-152.
25. Krajacic A., Ghosh M., Puentes R., Pearse D.D., Fouad K. Advantages of delaying the onset of rehabilitative reaching training in rats with incomplete spinal cord injury. Eur. J. Neurosci. 2009, 29:641-651.
26. Kuypers H.G. A new look at the organization of the motor system. Prog. Brain Res. 1982, 57:381-403.
27. Lang C.E., Schieber M.H. Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract. J. Neurophysiol. 2004, 91:1722-1733.
28. Lemon R.N. Descending pathways in motor control. Annu. Rev. Neurosci. 2008, 31:195-218.
29. Liebigt S., Schlegel N., Oberland J., Witte O.W., Redecker C., Keiner S. Effects of rehabilitative training and anti-inflammatory treatment on functional recovery and cellular reorganization following stroke. Exp. Neurol. 2012, 233:776-782.
30. Maldonado M.A., Allred R.P., Felthauser E.L., Jones T.A. 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.
31. Matelli M., Luppino G., Rizzolatti G. Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J. Comp. Neurol. 1991, 311:445-462.
32. Michaels R.L., Rothman S.M. Glutamate neurotoxicity in vitro: antagonist pharmacology and intracellular calcium concentrations. J. Neurosci. 1990, 10:283-292.
33. Murata Y., Higo N., Hayashi T.Y.M., Oishi T., Tsukada H., Isa T., Onoe H. Plastic changes in the ventral premotor area after primary motor cortex lesion in macaque monkeys: possible involvement in functional compensation of manual dexterity. Soc. Neurosci. Abstr. 2011, 1(279):222.
34. Murata Y., Higo N., Oishi T., Yamashita A., Matsuda K., Hayashi M., Yamane S. Effects of motor training on the recovery of manual dexterity after primary motor cortex lesion in macaque monkeys. J. Neurophysiol. 2008, 99:773-786.
35. Nishimura Y., Morichika Y., Isa T. A subcortical oscillatory network contributes to recovery of hand dexterity after spinal cord injury. Brain 2009, 132:709-721.
36. Nishimura Y., Onoe H., Morichika Y., Perfiliev S., Tsukada H., Isa T. Time-dependent central compensatory mechanisms of finger dexterity after spinal cord injury. Science 2007, 318:1150-1155.
37. 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 1996, 272:1791-1794.
38. Passingham R.E., Perry V.H., Wilkinson F. The long-term effects of removal of sensorimotor cortex in infant and adult rhesus monkeys. Brain 1983, 106:675-705.
39. Ramanathan D., Conner J.M., Tuszynski M.H. A form of motor cortical plasticity that correlates with recovery of function after brain injury. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:11370-11375.
40. Rosenzweig E.S., Courtine G., Jindrich D.L., Brock J.H., Ferguson A.R., Strand S.C., Nout Y.S., Roy R.R., Miller D.M., Beattie M.S., Havton L.A., Bresnahan J.C., Edgerton V.R., Tuszynski M.H. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat. Neurosci. 2010, 13:1505-1510.
41. Sasaki S., Isa T., Pettersson L.G., Alstermark B., Naito K., Yoshimura K., Seki K., Ohki Y. Dexterous finger movements in primate without monosynaptic corticomotoneuronal excitation. J. Neurophysiol. 2004, 92:3142-3147.
42. Schmidlin E., Wannier T., Bloch J., Rouiller E.M. Progressive plastic changes in the hand representation of the primary motor cortex parallel incomplete recovery from a unilateral section of the corticospinal tract at cervical level in monkeys. Brain Res. 2004, 1017:172-183.
43. Scivoletto G., Morganti B., Cosentino E., Molinari M. Utility of delayed spinal cord injury rehabilitation: an Italian study. Neurol. Sci. 2006, 27:86-90.
44. Sugiyama Y., Higo N., Yoshino-Saito K., Murata Y., Nishimura Y., Oishi T., Isa T. Effects of early versus late rehabilitative training on manual dexterity after corticospinal tract lesion in macaque monkeys. J. Neurophysiol. 2013, 109:2853-2865.
45. Terashima T., Ochiishi T., Yamauchi T. Immunohistochemical detection of calcium/calmodulin-dependent protein kinase II in the spinal cord of the rat and monkey with special reference to the corticospinal tract. J. Comp. Neurol. 1994, 340:469-479.
46. Twitchell T.E. The restoration of motor function following hemiplegia in man. Brain 1951, 74:443-480.
47. Vilensky J.A., Gilman S. Lesion of the precentral gyrus in nonhuman primates: a pre-medline bibliography. Int. J. Primatol. 2002, 23:1319-1333.
48. von Bonin G., Bailey P. The neocortex of Macaca mulatta. Illinois Monographs in the Medical Sciences 1947, 5:1-163. The University of Illinois Press, Urbana.
49. Wade D.T., Langton-Hewer R., Wood V.A., Skilbeck C.E., Ismail H.M. The hemiplegic arm after stroke: measurement and recovery. J. Neurol. Neurosurg. Psychiatry 1983, 46:521-524.
50. Wenzelburger R., Kopper F., Frenzel A., Stolze H., Klebe S., Brossmann A., Kuhtz-Buschbeck J., Golge M., Illert M., Deuschl G. Hand coordination following capsular stroke. Brain 2005, 128:64-74.
51. Wittenberg G.F., Schaechter J.D. The neural basis of constraint-induced movement therapy. Curr. Opin. Neurol. 2009, 22:582-588.
52. van den Brand R., Heutschi J., Barraud Q., DiGiovanna J., Bartholdi K., Huerlimann M., Friedli L., Vollenweider I., Moraud E.M., Duis S., Dominici N., Micera S., Musienko P., Courtine G. Restoring voluntary control of locomotion after paralyzing spinal cord injury. Science 2012, 336:1182-1185.
53. Yamamoto T., Oishi T., Higo N., Murayama S., Sato A., Takashima I., Sugiyama Y., Nishimura Y., Murata Y., Yoshino-Saito K., Isa T., Kojima T. Differential expression of secreted phosphoprotein 1 in the motor cortex among primate species and during postnatal development and functional recovery. PLoS ONE 2013, 8(5):e65701.