Reorganization and preservation of motor control of the brain in spinal cord injury: A systematic review

Journal of Neurotrauma

Volumn 26, Issue 11, 2009, Pages 2113-2126

  Kokotilo, Kristen J ^a,b   Eng, Janice J ^a,b   Curt, Armin ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Strong Rehab Centre   (Canada)

Author keywords

Motor; Neuroimaging; Plasticity; Reorganization; SCI

Indexed keywords

BRAIN FUNCTION; BRAIN MAPPING; CENTRAL NERVOUS SYSTEM; CHRONIC DISEASE; HUMAN; MOTOR CONTROL; NERVE CELL PLASTICITY; NEUROTRAUMATOLOGY; PARALYSIS; REVIEW; SPINAL CORD FUNCTION; SPINAL CORD INJURY; SYSTEMATIC REVIEW;

ADOLESCENT; ADULT; AGED; BRAIN; BRAIN MAPPING; HUMANS; MIDDLE AGED; NEURONAL PLASTICITY; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; YOUNG ADULT;

EID: 75449088122     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2008.0688     Document Type: Review

References (71)

1. Alkadhi, H., Brugger, P., Boendermaker, S.H., Crelier, G., Curt, A., Hepp-Reymond, M.C., and Kollias, S.S. (2005). What disconnection tells about motor imagery: evidence from paraplegic patients. Cereb. Cortex 15, 131-140.
2. Astolfi, L., Bakardjian, H., Cincotti, F., Mattia, D., Marciani, M.G., De Vico Fallani, F., Colosimo, A., Salinari, S., Miwakeichi, F., Yamaguchi, Y., Martinez, P., Cichocki, A., Tocci, A., and Babiloni, F. (2007). Estimate of causality between independent cortical spatial patterns during movement volition in spinal cord injured patients. Brain Topogr. 19, 107-123.
3. Baptiste, D.C., and Fehlings, M.G. (2006). Pharmacological approaches to repair the injured spinal cord. J. Neurotrauma 23, 318-334.
4. Bayona, N.A., Bitensky, J., and Teasell, R. (2005). Plasticity and reorganization of the uninjured brain. Top. Stroke Rehabil. 12, 1-10.
5. Beekhuizen, K.S., and Field-Fote, E.C. (2005). Massed practice versus massed practice with stimulation: Effects on upper extremity function and cortical plasticity in individuals with incomplete cervical spinal cord injury. Neurorehabil. Neural Repair 19, 33-45.
6. Beekhuizen, K.S., and Field-Fote, E.C. (2008). Sensory stimulation augments the effects of massed practice training in persons with tetraplegia. Arch. Phys. Med. Rehabil. 89, 602-608.
7. Beric, A., and Raghavan, M. (2004). Transcranial electrical and magnetic stimulation, in: Electroencephalography. Basic Principles, Clinical Applications and Related Fields, 5th ed. E. Niedermeyer and F.H. Loepes Da Silva (eds). Lippincott Williams & Wilkins: Philadelphia, pps. 857-880.
8. Brasil-Neto, J.P., Cohen, L.G., Pascual-Leone, A., Jabir, F.K., Wall, R.T., and Hallett, M. (1992). Rapid reversible modulation of human motor outputs after transient deafferentation of the forearm: a study with transcranial magnetic stimulation. Neurology 42, 1302-1306.
9. Brasil-Neto, J.P., Valls-Sole, J., Pascual-Leone, A., Cammarota, A., Amassian, V.E., Cracco, R., Hallett, M., and Cohen, L.G. (1993). Rapid modulation of human cortical motor outputs following ischaemic nerve block. Brain 116, 511-525.
10. Bruehlmeier, M., Dietz, V., Leenders, K.L., Roelcke, U., Missimer, J., and Curt, A. (1998). How does the human brain deal with a spinal cord injury? Eur. J. Neurosci. 10, 3918-3922.
11. Canadian Paraplegic Association. (2008). SCI Facts. Retrieved June 6, 2008: http:==www.canparaplegic.org=en=SCI-Facts- 67.html
12. Castro, A., Diaz, F., and van Boxtel, G.J. (2007). How does a short history of spinal cord injury affect movement-related brain potentials? Eur. J. Neurosci. 25, 2927-2934.
13. Ceballos-Baumann, A.O. (2003). Functional imaging in Parkinson's disease: activation studies with PET, fMRI and SPECT. J. Neurol. 250 (Suppl 1), 115-123.
14. Cramer, S.C., Lastra, L., Lacourse, M.G., and Cohen, M.J. (2005). Brain motor system function after chronic, complete spinal cord injury. Brain 128, 2941-2950.
15. Cramer, S.C., Nelles, G., Benson, R.R., Kaplan, J.D., Parker, R.A., Kwong, K.K., Kennedy, D.N., Finklestein, S.P., and Rosen, B.R. (1997). A functional MRI study of subjects recovered from hemiparetic stroke. Stroke 28, 2518-2527.
16. Cramer, S.C., Orr, E.L., Cohen, M.J., and Lacourse, M.G. (2007). Effects of motor imagery training after chronic, complete spinal cord injury. Exp. Brain Res. 177, 233-242.
17. Cramer, S.C., Weisskoff, R.M., Schaechter, J.D., Nelles, G., Foley, M., Finklestein, S.P., and Rosen, B.R. (2002). Motor cortex activation is related to force of squeezing. Hum. Brain Mapp. 16, 197-205.
18. Curt, A., Alkadhi, H., Crelier, G.R., Boendermaker, S.H., Hepp-Reymond, M.C., and Kollias, S.S. (2002a). Changes of nonaffected upper limb cortical representation in paraplegic patients as assessed by fMRI. Brain 125, 2567-2578.
19. Curt, A., Bruehlmeier, M., Leenders, K.L., Roelcke, U., and Dietz, V. (2002b). Differential effect of spinal cord injury and functional impairment on human brain activation. J. Neurotrauma 19, 43-51.
20. Dai, T.H., Liu, J.Z., Sahgal, V., Brown, R.W., and Yue, G.H. (2001). Relationship between muscle output and functional MRI-measured brain activation. Exp. Brain Res. 140, 290-300.
21. Dettmers, C., Fink, G.R., Lemon, R.N., Stephan, K.M., Passingham, R.E., Silbersweig, D., Holmes, A., Ridding, M.C., Brooks, D.J., and Frackowiak, R.S. (1995). Relation between cerebral activity and force in the motor areas of the human brain. J. Neurophysiol. 74, 802-815.
22. Dettmers, C., Ridding, M.C., Stephan, K.M., Lemon, R.N., Rothwell, J.C., and Frackowiak, R.S. (1996). Comparison of regional cerebral blood flow with transcranial magnetic stimulation at different forces. J. Appl. Physiol. 81, 596-603.
23. Donoghue, J.P., Suner, S., and Sanes, J.N. (1990). Dynamic organization of primary motor cortex output to target muscles in adult rats. II. Rapid reorganization following motor nerve lesions. Exp. Brain Res. 79, 492-503.
24. Dunlop, S.A. (2008). Activity-dependent plasticity: implications for recovery after spinal cord injury. Trends Neurosci. 31, 410-418.
25. Fallani, F.D., Astolfi, L., Cincotti, F., Mattia, D., Marciani, M.G., Salinari, S., Kurths, J., Gao, S., Cichocki, A., Colosimo, A., and Babiloni, F. (2007). Cortical functional connectivity networks in normal and spinal cord injured patients: evaluation by graph analysis. Hum. Brain Mapp. 28, 1334-1346.
26. Flanagan, J.R., and Wing, A.M. (1997). The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J. Neurosci. 17, 1519-1528.
27. Frost, S.B., Barbay, S., Friel, K.M., Plautz, E.J., and Nudo, R.J. (2003). Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. J. Neurophysiol. 89, 3205-3214.
28. Gandevia, S.C., Macefield, G., Burke, D., and McKenzie, D.K. (1990). Voluntary activation of human motor axons in the absence of muscle afferent feedback the control of the deafferented hand. Brain 113, 1563-1581.
29. Green, J.B., Sora, E., Bialy, Y., Ricamato, A., and Thatcher, R.W. (1999). Cortical motor reorganization after paraplegia: an EEG study. Neurology 53, 736-743.
30. Green, J.B., Sora, E., Bialy, Y., Ricamato, A., and Thatcher, R.W. (1998). Cortical sensorimotor reorganization after spinal cord injury: an electroencephalographic study. Neurology 50, 1115-1121.
31. Gregory, C.M., Bowden, M.G., Jayaraman, A., Shah, P., Behrman, A., Kautz, S.A., and Vandenborne, K. (2007). Resistance training and locomotor recovery after incomplete spinal cord injury: a case series. Spinal Cord 45, 522-530.
32. Guest, J., Herrera, L.P., and Qian, T. (2006). Rapid recovery of segmental neurological function in a tetraplegic patient following transplantation of fetal olfactory bulb-derived cells. Spinal Cord 44, 135-142.
33. Halder, P., Curt, A., Brem, S., Lang-Dullenkopf, A., Bucher, K., Kollias, S., and Brandeis, D. (2006). Preserved aspects of cortical foot control in paraplegia. Neuroimage 31, 692-698.
34. Hamdy, S., Rothwell, J.C., Aziz, Q., Singh, K.D., and Thompson, D.G. (1998). Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat. Neurosci. 1, 64-68.
35. Hicks, A.L., Adams, M.M., Martin Ginis, K., Giangregorio, L., Latimer, A., Phillips, S.M., and McCartney, N. (2005). Longterm body-weight-supported treadmill training and subsequent follow-up in persons with chronic SCI: effects on functional walking ability and measures of subjective wellbeing. Spinal Cord 43, 291-298.
36. Hoffman, L.R., and Field-Fote, E.C. (2007). Cortical reorganization following bimanual training and somatosensory stimulation in cervical spinal cord injury: a case report. Phys. Ther. 87, 208-223.
37. Hotz-Boendermaker, S., Funk, M., Summers, P., Brugger, P., Hepp-Reymond, M.C., Curt, A., and Kollias, S.S. (2008). Preservation of motor programs in paraplegics as demonstrated by attempted and imagined foot movements. Neuroimage 39, 383-394.
38. Jain, N., Catania, K.C., and Kaas, J.H. (1997). Deactivation and reactivation of somatosensory cortex after dorsal spinal cord injury. Nature 386, 495-498.
39. Jeannerod, M., Michel, F., and Prablanc, C. (1984). The control of hand movements in a case of hemianaesthesia following a parietal lesion. Brain107, 899-920.
40. Jurkiewicz, M.T., Mikulis, D.J., McIlroy, W.E., Fehlings, M.G., and Verrier, M.C. (2007). Sensorimotor cortical plasticity during recovery following spinal cord injury: a longitudinal FMRI study. Neurorehabil. Neural Repair 21, 527-538.
41. Kolb, B. (1995). Brain Plasticity and Behavior. Lawrence Erlbaum: Mahwah, NJ.
42. Kossev, A., Siggelkow, S., Schubert, M., Wohlfarth, K., and Dengler, R. (1999). Muscle vibration: different effects on transcranial magnetic and electrical stimulation. Muscle Nerve 22, 946-948.
43. Kwon, B.K., Liu, J., Messerer, C., Kobayashi, N.R., McGraw, J., Oschipok, L., and Tetzlaff, W. (2002). Survival and regeneration of rubrospinal neurons 1 year after spinal cord injury. Proc. Natl. Acad. Sci. USA 99, 3246-3251. (Pubitemid 34240617)
44. Lacourse, M.G., Cohen, M.J., Lawrence, K.E., and Romero, D.H. (1999). Cortical potentials during imagined movements in individuals with chronic spinal cord injuries. Behav. Brain Res. 104, 73-88.
45. Lotze, M., Laubis-Herrmann, U., and Topka, H. (2006). Combination of TMS and fMRI reveals a specific pattern of reorganization in M1 in patients after complete spinal cord injury. Restor. Neurol. Neurosci. 24, 97-107.
46. Lotze, M., Laubis-Herrmann, U., Topka, H., Erb, M., and Grodd, W. (1999). Reorganization in the primary motor cortex after spinal cord injury-a functional magnetic resonance (fMRI) study. Restor. Neurol. Neurosci. 14, 183-187.
47. Macefield, V.G., Gandevia, S.C., Bigland-Ritchie, B., Gorman, R.B., and Burke, D. (1993). The firing rates of human motoneurones voluntarily activated in the absence of muscle afferent feedback. J. Physiol. 471, 429-443.
48. Mattia, D., Cincotti, F., Mattiocco, M., Scivoletto, G., Marciani, M.G., and Babiloni, F. (2006). Motor-related cortical dynamics to intact movements in tetraplegics as revealed by highresolution EEG. Hum. Brain Mapp. 27, 510-519.
49. Maynard, F.M., Jr., Bracken, M.B., Creasey, G., Ditunno, J.F., Jr., Donovan, W.H., Ducker, T.B., Garber, S.L., Marino, R.J., Stover, S.L., Tator, C.H., Waters, R.L., Wilberger, J.E., and Young, W. (1997). International standards for neurological and functional classification of spinal cord injury. American Spinal Injury Association. Spinal Cord 35, 266-274.
50. Merzenich, M.M., Nelson, R.J., Stryker, M.P., Cynader, M.S., Schoppmann, A., and Zook, J.M. (1984). Somatosensory cortical map changes following digit amputation in adult monkeys. J. Comp. Neurol. 224, 591-605.
51. Mikulis, D.J., Jurkiewicz, M.T., McIlroy, W.E., Staines, W.R., Rickards, L., Kalsi-Ryan, S., Crawley, A.P., Fehlings, M.G., and Verrier, M.C. (2002). Adaptation in the motor cortex following cervical spinal cord injury. Neurology 58, 794-801.
52. Nielsen, J.B., and Sinkjaer, T. (2002). Afferent feedback in the control of human gait. J. Electromyogr. Kinesiol. 12, 213-217.
53. Nowak, D.A., Glasauer, S., and Hermsdörfer, J. (2003). Grip force efficiency in long-term deprivation of somatosensory feedback. Neuroreport 14, 1803-1807.
54. Raineteau, O., and Schwab, M.E. (2001). Plasticity of motor systems after incomplete spinal cord injury. Nat. Rev. Neurosci. 2, 263-273.
55. Sabbah, P., de Schonen, S., Leveque, C., Gay, S., Pfefer, F., Nioche, C., Sarrazin, J.L., Barouti, H., Tadie, M., and Cordoliani, Y.S. (2002). Sensorimotor cortical activity in patients with complete spinal cord injury: a functional magnetic resonance imaging study. J. Neurotrauma 19, 53-60.
56. Shoham, S., Halgren, E., Maynard, E.M., and Normann, R.A. (2001). Motor-cortical activity in tetraplegics. Nature 413, 793.
57. Swayne, O., Rothwell, J., and Rosenkranz, K. (2006). Transcallosal sensorimotor integration: effects of sensory input on cortical projections to the contralateral hand. Clin. Neurophysiol. 117, 855-863.
58. Teasell, R., Bayona, N.A., and Bitensky, J. (2005). Plasticity and reorganization of the brain post stroke. Top. Stroke Rehabil. 12, 11-26. (Pubitemid 41233410)
59. Turner, J.A., Lee, J.S., Martinez, O., Medlin, A.L., Schandler, S.L., and Cohen, M.J. (2001). Somatotopy of the motor cortex after long-term spinal cord injury or amputation. IEEE Trans. Neural Syst. Rehabil. Eng. 9, 154-160.
60. Turner, J.A., Lee, J.S., Schandler, S.L., and Cohen, M.J. (2003). An fMRI investigation of hand representation in paraplegic humans. Neurorehabil. Neural Repair 17, 37-47.
61. Ward, N.S., Brown, M.M., Thompson, A.J., and Frackowiak, R.S. (2003). Neural correlates of outcome after stroke: a crosssectional fMRI study. Brain 126, 1430-1448.
62. Weiller, C., Chollet, F., Friston, K.J., Wise, R.J., and Frackowiak, R.S. (1992). Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann. Neurol. 31, 463-472.
63. Weiller, C., May, A., Sach, M., Buhmann, C., and Rijntjes, M. (2006). Role of functional imaging in neurological disorders. J. Magn. Reson. Imaging 23, 840-850.
64. Werhahn, K.J., Mortensen, J., Kaelin-Lang, A., Boroojerdi, B., and Cohen, L.G. (2002). Cortical excitability changes induced by deafferentation of the contralateral hemisphere. Brain 125, 1402-1413.
65. Winchester, P., McColl, R., Querry, R., Foreman, N., Mosby, J., Tansey, K., and Williamson, J. (2005). Changes in supraspinal activation patterns following robotic locomotor therapy in motor-incomplete spinal cord injury. Neurorehabil. Neural Repair 19, 313-324.
66. Wirz, M., Zemon, D.H., Rupp, R., Scheel, A., Colombo, G., Dietz, V., and Hornby, T.G. (2005). Effectiveness of automated locomotor training in patients with chronic incomplete spinal cord injury: a multicenter trial. Arch. Phys. Med. Rehabil. 86, 672-680.
67. Wolpaw, J.R. (2007). Spinal cord plasticity in acquisition and maintenance of motor skills. Acta Physiol. 189, 155-169.
68. Wolpert, D.M., Ghahramani, Z., and Jordan, M.I. (1995). An internal model for sensorimotor integration. Science 269, 1880-1882.
69. Wyndaele, M., and Wyndaele, J.J. (2006). Incidence, prevalence and epidemiology of spinal cord injury: what learns a worldwide literature survey? Spinal Cord 44, 523-529.
70. Yu, D. (1998). A crash course in spinal cord injury. Postgrad. Med. 104, 109-110, 113-116, 119-122.
71. Ziemann, U., Corwell, B., and Cohen, L.G. (1998). Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J. Neurosci. 18, 1115-1123.