Minimal forced use without constraint stimulates spontaneous use of the impaired upper extremity following motor cortex injury

Experimental Brain Research

Volumn 202, Issue 3, 2010, Pages 529-542

  Darling, Warren G ^a   Pizzimenti, Marc A ^a   Rotella, Diane L ^a   Hynes, Stephanie M ^a   Ge, Jizhi ^b   Stilwell Morecraft, Kimberly S ^b   Vanadurongvan, Tyler ^b   McNeal, David W ^b   Solon Cline, Kathryn M ^b   Morecraft, Robert J ^b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

Brain injury; Dexterity; Hand; Motor recovery; Therapeutic intervention

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; CONVALESCENCE; FEMALE; FRONTAL LOBE; HEMISPHERIC DOMINANCE; LIMB MOVEMENT; MACACA; MALE; MOTOR CONTROL; MOTOR CORTEX; MOTOR PERFORMANCE; NONHUMAN; PRIORITY JOURNAL; TASK PERFORMANCE;

ANIMALS; ARM; BRAIN INJURIES; DISEASE MODELS, ANIMAL; EXERCISE THERAPY; FEMALE; FUNCTIONAL LATERALITY; MACACA MULATTA; MALE; MOTOR CORTEX; PARESIS; RANDOM ALLOCATION; RECOVERY OF FUNCTION;

EID: 77951093171     PISSN: 00144819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00221-010-2157-y     Document Type: Article

References (66)

1. D Boussaoud J Tanne-Gariepy T Wannier EM Rouiller 2005 Callosal connections of dorsal versus ventral premotor areas in the macaque monkey: a multiple retrograde tracing study BMC Neurosci 6 67 10.1186/1471-2202-6-67 16309550 (Pubitemid 41762659)
2. C Brogardh M Vestling BH Sjolund 2009 Shortened constraint-induced movement therapy in subacute stroke - no effect of using a restraint: a randomized controlled study with independent observers J Rehabil Med 41 231 236 10.2340/16501977-0312 19247541
3. RB Chamoun MA Mikati YG Comair 2007 Functional recovery following resection of an epileptogenic focus in the motor hand area Epilepsy Behav 11 384 388 10.1016/j.yebeh.2007.05.015 17709300 (Pubitemid 350048473)
4. MD Crocker M MacKay-Lyons E McDonnell 1997 Forced use of the upper extremity in cerebral palsy: a single-case design Am J Occup Ther 51 824 833 1:STN:280:DyaK1c%2FlsF2mtg%3D%3D 9394143
5. WG Darling CR Peterson JL Herrick DW McNeal KS Stilwell-Morecraft RJ Morecraft 2006 Measurement of coordination of object manipulation in non-human primates J Neurosci Methods 154 38 44 10.1016/j.jneumeth.2005.11.013 16464505 (Pubitemid 43816711)
6. Darling WG, Pizzimenti MA, Hynes SM, Rotella D, Headley G, Ge J, McNeal DW, Stilwell-Morecraft KS, Vanadurongvan T, Morecraft RJ (2009a) Recovery of ipsilesional hand fine motor function following motor cortex lesions in rhesus monkeys. Society for Neuroscience 2009 Abstract Viewer #768.12
7. WG Darling MA Pizzimenti DL Rotella CR Peterson SM Hynes J Ge K Solon DW McNeal KS Stilwell-Morecraft RJ Morecraft 2009 Volumetric effects of motor cortex injury on recovery of dexterous movements Exp Neurol 220 90 108 10.1016/j.expneurol.2009.07.034 19679127
8. J Duque N Murase P Celnik F Hummel M Harris-Love R Mazzocchio E Olivier LG Cohen 2007 Intermanual differences in movement-related interhemispheric inhibition J Cogn Neurosci 19 204 213 10.1162/jocn.2007.19.2.204 17280510 (Pubitemid 46220703)
9. F Fregni PS Boggio AC Valle RR Rocha J Duarte MJ Ferreira T Wagner S Fecteau SP Rigonatti M Riberto SD Freedman A Pascual-Leone 2006 A sham-controlled trial of a 5-day course of repetitive transcranial magnetic stimulation of the unaffected hemisphere in stroke patients Stroke 37 2115 2122 10.1161/01.STR.0000231390.58967.6b 16809569 (Pubitemid 44309913)
10. S Geyer M Matelli G Luppino K Zilles 2000 Functional neuroanatomy of the primate isocortical motor system Anat Embryol 202 443 474 10.1007/s004290000127 1:STN:280:DC%2BD3M7gsV2rtQ%3D%3D 11131014
11. CE Han MA Arbib N Schweighofer 2008 Stroke rehabilitation reaches a threshold PLoS Comput Biol 4 e1000133 10.1371/journal.pcbi.1000133 18769588
12. JE Harris JJ Eng 2006 Individuals with the dominant hand affected following stroke demonstrate less impairment than those with the nondominant hand affected Neurorehabil Neural Repair 20 380 389 10.1177/1545968305284528 16885424 (Pubitemid 44154884)
13. R Heffner B Masterton 1975 Variation in form of the pyramidal tract and its relationship to digital dexterity Brain Behav Evol 12 161 200 10.1159/000124401 1:STN:280:DyaE287hsFOgug%3D%3D 1212616
14. RS Heffner RB Masterton 1983 The role of the corticospinal tract in the evolution of human digital dexterity Brain Behav Evol 23 165 183 10.1159/000121494 1:STN:280:DyaL2c7ivFCjuw%3D%3D 6667369
15. I Kermadi Y Liu A Tempini EM Rouiller 1997 Effects of reversible inactivation of the supplementary motor area (SMA) on unimanual grasp and bimanual pull and grasp performance in monkeys Somatosens Mot Res 14 268 280 10.1080/08990229770980 1:STN:280:DyaK1c7gsFGkug%3D%3D 9443367 (Pubitemid 28017836)
16. D Kimura 1982 Left-hemisphere control of oral and brachial movements and their relation to communication Philos Trans R Soc Lond B Biol Sci 298 135 149 10.1098/rstb.1982.0077 1:STN:280:DyaL383nsFCgsw%3D%3D 6125966
17. D Kimura Y Archibald 1974 Motor functions of the left hemisphere Brain 97 337 350 10.1093/brain/97.1.337 1:STN:280:DyaE2M%2Fls1Snsg%3D%3D 4434181
18. HD Knapp E Taub AJ Berman 1959 Conditioned response following deafferentation in the monkey Trans Am Neurol Assoc 84 185 187 1:STN:280:DyaF3c7mt1Kquw%3D%3D 14410055
19. HD Knapp E Taub AJ Berman 1963 Movements in monkeys with deafferented forelimbs Exp Neurol 7 305 315 10.1016/0014-4886(63)90077-3 1:STN:280: DyaF383isFOhtg%3D%3D 14033714
20. S Knecht B Drager M Deppe L Bobe H Lohmann A Floel EB Ringelstein H Henningsen 2000 Handedness and hemispheric language dominance in healthy humans Brain 123 Pt 12 2512 2518 10.1093/brain/123.12.2512 11099452
21. Kuypers H (1981) Anatomy of the descending motor pathways. In: Brooks VB (ed) Handbook of physiology section 1, the nervous system, vol II. motor control, pt I. American physiological society, Bethesda, pp 567-666
22. D Laplane J Talairach V Meininger J Bancaud A Bouchareine 1977 Motor consequences of motor area ablations in man J Neurol Sci 31 29 49 10.1016/0022-510X(77)90004-1 1:STN:280:DyaE2s%2Fps1Siug%3D%3D 833609 (Pubitemid 8017909)
23. D Laplane J Talairach V Meininger J Bancaud JM Orgogozo 1977 Clinical consequences of corticectomies involving the supplementary motor area in man J Neurol Sci 34 301 314 10.1016/0022-510X(77)90148-4 1:STN:280: DyaE1c%2FmvVahsA%3D%3D 591992 (Pubitemid 8230911)
24. RA Lehman 1980 The handedness of rhesus monkeys. III. Consistency within and across activities Cortex 16 197 204 1:STN:280:DyaL3M7js12ltg%3D%3D 7471760
25. RA Lehman 1989 Hand preferences of rhesus monkeys on differing tasks Neuropsychologia 27 1193 1196 10.1016/0028-3932(89)90102-4 1:STN:280: DyaK3c%2FksVOisQ%3D%3D 2812302 (Pubitemid 19256787)
26. RN Lemon J Griffiths 2005 Comparing the function of the corticospinal system in different species: organizational differences for motor specialization? Muscle Nerve 32 261 279 10.1002/mus.20333 15806550 (Pubitemid 41232610)
27. RN Lemon GW Mantel RB Muir 1986 Corticospinal facilitation of hand muscles during voluntary movement in the conscious monkey J Physiol 381 497 527 1:STN:280:DyaL2szhtFajsQ%3D%3D 3625543
28. MF Levin LA Knaut EC Magdalon S Subramanian 2009 Virtual reality environments to enhance upper limb functional recovery in patients with hemiparesis Stud Health Technol Inform 145 94 108 19592789
29. J Liu A Morel T Wannier EM Rouiller 2002 Origins of callosal projections to the supplementary motor area (SMA): a direct comparison between pre-SMA and SMA-proper in macaque monkeys J Comp Neurol 443 71 85 10.1002/cne.10087 11793348 (Pubitemid 34027570)
30. CG Mansur F Fregni PS Boggio M Riberto J Gallucci-Neto CM Santos T Wagner SP Rigonatti MA Marcolin A Pascual-Leone 2005 A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients Neurology 64 1802 1804 10.1212/01.WNL.0000161839.38079.92 1:STN:280:DC%2BD2M3mvFOhtg%3D%3D 15911819 (Pubitemid 40695826)
31. CR Mason LE Miller JF Baker JC Houk 1998 Organization of reaching and grasping movements in the primate cerebellar nuclei as revealed by focal muscimol inactivations J Neurophysiol 79 537 554 1:STN:280:DyaK1c7jtVKgsQ%3D%3D 9463420
32. DW McNeal WG Darling J Ge KS Stilwell-Morecraft K Solon SM Hynes MA Pizzimenti D Rotella T Vanadurongvan RJ Morecraft 2010 Selective long-term reorganization of the corticospinal projection from the supplementary motor cortex following recovery from lateral motor cortex injury J Comp Neurol 518 586 621 10.1002/cne.22218 20034062
33. N Mikuni A Ikeda H Yoneko S Amano T Hanakawa H Fukuyama N Hashimoto 2005 Surgical resection of an epileptogenic cortical dysplasia in the deep foot sensorimotor area Epilepsy Behav 7 559 562 10.1016/j.yebeh.2005.07.016 16194627 (Pubitemid 41614157)
34. RJ Morecraft JL Louie JL Herrick KS Stilwell-Morecraft 2001 Cortical innervation of the facial nucleus in the non-human primate: a new interpretation of the effects of stroke and related subtotal brain trauma on the muscles of facial expression Brain 124 176 208 10.1093/brain/124.1.176 1:STN:280: DC%2BD3M7gvV2itw%3D%3D 11133797
35. RJ Morecraft JL Herrick KS Stilwell-Morecraft JL Louie CM Schroeder JG Ottenbacher MW Schoolfield 2002 Localization of arm representation in the corona radiata and internal capsule in the non-human primate Brain 125 176 198 10.1093/brain/awf011 11834603
36. RJ Morecraft DW McNeal KS Stilwell-Morecraft Z Dvanajscak J Ge P Schneider 2007 Localization of arm representation in the cerebral peduncle of the non-human primate J Comp Neurol 504 149 167 10.1002/cne.21438 17626268 (Pubitemid 47327475)
37. RJ Morecraft DW McNeal KS Stilwell-Morecraft M Gedney J Ge CM Schroeder GW Van Hoesen 2007 Amygdala interconnections with the cingulate motor cortex in the rhesus monkey J Comp Neurol 500 134 165 10.1002/cne.21165 17099887 (Pubitemid 44904306)
38. SM Morton CE Lang AJ Bastian 2001 Inter- and intra-limb generalization of adaptation during catching Exp Brain Res 141 438 445 10.1007/s002210100889 1:STN:280:DC%2BD38%2FotlSksA%3D%3D 11810138 (Pubitemid 33145102)
39. Y Murata N Higo T Oishi A Yamashita K Matsuda M Hayashi S Yamane 2008 Effects of motor training on the recovery of manual dexterity after primary motor cortex lesion in macaque monkeys J Neurophysiol 99 773 786 10.1152/jn.01001.2007 18094104 (Pubitemid 351253234)
40. Nagamoto-Combs K, McNeal DW, Morecraft RJ, Combs CK (2007) Prolonged microgliosis in the rhesus monkey central nervous system after traumatic brain injury. J Neurotrauma 24:1719-1742
41. Nagamoto-Combs K, Morecraft RJ, Darling WG, Combs C (2009) Long-term gliosis and molecular changes in the cervical spinal cord of the rhesus monkey after traumatic brain injury. J Neurotrauma (in press)
42. RJ Nudo GW Milliken 1996 Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys J Neurophysiol 75 2144 2149 1:STN:280:DyaK28zhslahsA%3D%3D 8734610
43. R Nudo W Jenkins M Merzenich T Prejean R Grenda 1992 Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys J Neurosci 12 2918 2947 1:STN:280:DyaK38zls1WrtQ%3D%3D 1494940
44. R Ogden SI Franz 1917 On cerebral motor control: the recovery from experimentally produced hemiplegia Psychobiology 1 33 47 10.1037/h0074814
45. DN Pandya LA Vignolo 1971 Intra- and interhemispheric projections of the precentral, premotor and arcuate areas in the rhesus monkey Brain Res 26 217 233 1:STN:280:DyaE3M7jtF2mug%3D%3D 4993847
46. N Picard PL Strick 1996 Motor areas of the medial wall: a review of their location and functional activation Cereb Cortex 6 342 353 10.1093/cercor/6.3. 342 1:STN:280:DyaK28zisVaqsg%3D%3D 8670662 (Pubitemid 26161547)
47. MA Pizzimenti WG Darling DL Rotella DW McNeal JL Herrick J Ge KS Stilwell-Morecraft RJ Morecraft 2007 Measurement of reaching kinematics and prehensile dexterity in nonhuman primates J Neurophysiol 98 1015 1029 10.1152/jn.00354.2007 17553948 (Pubitemid 47236050)
48. K Quencer MS Okun G Crucian HH Fernandez F Skidmore KM Heilman 2007 Limb-kinetic apraxia in Parkinson disease Neurology 68 150 151 10.1212/01.wnl.0000250331.35912.a5 1:STN:280:DC%2BD2s%2FhsFSisQ%3D%3D 17151340 (Pubitemid 46071901)
49. PE Roland K Zilles 1996 Functions and structures of the motor cortices in humans Curr Opin Neurobiol 6 773 781 10.1016/S0959-4388(96)80027-4 1:CAS:528:DyaK2sXhtVOku70%3D 9000024 (Pubitemid 27052918)
50. RC Rostomily MS Berger GA Ojemann E Lettich 1991 Postoperative deficits and functional recovery following removal of tumors involving the dominant hemisphere supplementary motor area J Neurosurg 75 62 68 10.3171/jns.1991.75.1. 0062 1:STN:280:DyaK3M3lvFamsQ%3D%3D 2045920
51. RL Sainburg J Wang 2002 Interlimb transfer of visuomotor rotations: independence of direction and final position information Exp Brain Res 145 437 447 10.1007/s00221-002-1140-7 12172655 (Pubitemid 34994786)
52. KC Sato J Tanji 1989 Digit-muscle responses evoked from multiple intracortical foci in monkey precentral motor cortex J Neurophysiol 62 959 970 1:STN:280:DyaK3c%2FjvFCqtw%3D%3D 2681562
53. MH Schieber 2007 Chapter 2 comparative anatomy and physiology of the corticospinal system Handb Clin Neurol 82 15 37 10.1016/S0072-9752(07)80005-4 18808887
54. M Sivak C Mavroidis MK Holden 2009 Design of a low cost multiple user virtual environment for rehabilitation (MUVER) of patients with stroke Stud Health Technol Inform 142 319 324 19377177
55. E Taub SJ Ellman AJ Berman 1966 Deafferentation in monkeys: effect on conditioned grasp response Science 151 593 594 10.1126/science.151.3710.593 1:STN:280:DyaF28%2FnvFCmsw%3D%3D 4955315
56. E Taub IA Goldberg P Taub 1975 Deafferentation in monkeys: pointing at a target without visual feedback Exp Neurol 46 178 186 10.1016/0014-4886(75)90040- 0 1:STN:280:DyaE2M%2Flsl2nug%3D%3D 1109336
57. E Taub RD Heitmann G Barro 1977 Alertness, level of activity, and purposive movement following somatosensory deafferentation in monkeys Ann N Y Acad Sci 290 348 365 10.1111/j.1749-6632.1977.tb39737.x 1:STN:280: DyaE1c3gvFalug%3D%3D 96722
58. Taub E, Miller NE, Novack TA, Cook EW 3rd, Fleming WC, Nepomuceno CS, Connell JS, Crago JE (1993) Technique to improve chronic motor deficit after stroke. Arch Phys Med Rehabil 74:347-354
59. E Taub G Uswatte VW Mark DM Morris 2006 The learned nonuse phenomenon: implications for rehabilitation Eura Medicophys 42 241 256 1:STN:280: DC%2BD28ngs1SrtQ%3D%3D 17039223
60. AA Timmermans HA Seelen RD Willmann H Kingma 2009 Technology-assisted training of arm-hand skills in stroke: concepts on reacquisition of motor control and therapist guidelines for rehabilitation technology design J Neuroeng Rehabil 6 1 10.1186/1743-0003-6-1 19154570
61. J Wang RL Sainburg 2003 Mechanisms underlying interlimb transfer of visuomotor rotations Exp Brain Res 149 520 526 12677333
62. CJ Winstein DK Rose SM Tan R Lewthwaite HC Chui SP Azen 2004 A randomized controlled comparison of upper-extremity rehabilitation strategies in acute stroke: a pilot study of immediate and long-term outcomes Arch Phys Med Rehabil 85 620 628 10.1016/j.apmr.2003.06.027 15083439 (Pubitemid 38881052)
63. SL Wolf DE Lecraw LA Barton BB Jann 1989 Forced use of hemiplegic upper extremities to reverse the effect of learned nonuse among chronic stroke and head-injured patients Exp Neurol 104 125 132 10.1016/S0014-4886(89)80005-6 1:STN:280:DyaL1M3htFajtA%3D%3D 2707361 (Pubitemid 19122839)
64. SL Wolf CJ Winstein JP Miller E Taub G Uswatte D Morris C Giuliani KE Light D Nichols-Larsen for the EI 2006 Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial JAMA 296 2095 2104 10.1001/jama.296.17.2095 1:CAS:528:DC%2BD28XhtFKrurfP 17077374 (Pubitemid 44664704)
65. SL Wolf CJ Winstein JP Miller PA Thompson E Taub G Uswatte D Morris S Blanton D Nichols-Larsen PC Clark 2008 Retention of upper limb function in stroke survivors who have received constraint-induced movement therapy: the EXCITE randomised trial Lancet Neurol 7 33 40 10.1016/S1474-4422(07)70294-6 18077218 (Pubitemid 50013946)
66. K Zilles G Schlaug M Matelli G Luppino A Schleicher M Qu A Dabringhaus R Seitz PE Roland 1995 Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data J Anat 187 Pt 3 515 537 1:CAS:528:DyaK28XhtFKltr8%3D 8586553