Incomplete spinal cord injury: Neuronal mechanisms of motor recovery and hyperreflexia

Archives of Physical Medicine and Rehabilitation

Volumn 80, Issue 5, 1999, Pages 587-599

  Little, James W ^a,c   Ditunno Jr , John F ^a,d   Stiens, Steven A ^a,c   Harris, Roger M ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTONOMIC HYPERREFLEXIA; CERVICAL SPINAL CORD INJURY; DEPOLARIZATION; HUMAN; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROTRANSMISSION; REFLEX; REVIEW; SPINAL CORD INJURY;

EID: 0032899990     PISSN: 00039993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0003-9993(99)90204-6     Document Type: Review

References (119)

1. Ditunno JF Jr, Cohen ME, Formal C, Whiteneck GG. Functional outcomes. In: Stover SL, DeLisa JA, Whiteneck GG, editors. Spinal cord injury: clinical outcomes from the model systems. Gaithersburg (MD): Aspen Publishers; 1995. p. 170-84.
2. Burns SP, Golding DG, Rolle WA, Graziani V, Ditunno JF Jr. Recovery of ambulation in motor-incomplete tetraplegia. Arch Phys Med Rehabil 1997;78:1169-72.
3. Blight AR. Remyelination, revascularization and recovery of function in experimental spinal cord injury. Adv Neurol 1993;59: 91-104.
4. Young W. Nonregenerative approaches to spinal cord injury. In: Gorio A, editor. Neuroregeneration. New York: Raven Press; 1993. p. 169-84.
5. Taylor J, editor. Selected writings of John Hughlings Jackson. New York: Basic Books; 1958.
6. Pike FH, Elsberg CA, McCulloch WS, Rizzolo A. Some observations on experimentally produced convulsions: the localization of the motor mechanisms from which the typical clonic movements of epilepsy arise. Am J Psychiatry 1929;9:259-83.
7. Nathan PW, Smith MC. Effects of two unilateral cordotomies on the motility of the lower limb. Brain 1973;96:471-94.
8. Little JW, Harris RM, Sohlberg RC. Locomotor recovery following subtotal spinal cord lesions in a rat model. Neurosci Lett 1988;87:189-94.
9. Helgren ME, Goldberger ME. The recovery of postural reflexes and locomotion following low thoracic hemisection in adult cats involves compensation by undamaged primary afferent pathways. Exp Neurol 1993;123:17-34.
10. Eidelberg E. Consequences of spinal cord lesions upon motor function, with special reference to locomotor activity. Prog Neurobiol 1981;17:185-202.
11. Galea MP, Darian-Smith I. Manual dexterity and corticospinal connectivity following unilateral section of the cervical spinal cord in the macaque monkey. J Comp Neurol 1997;381:307-19.
12. Little JW, Halar E. Temporal course of motor recovery after Brown-Séquard spinal cord injuries. Paraplegia 1985;23:39-46.
13. Ditunno JF, Graziani V, Tessler A. Neurological assessment in spinal cord injury. In: Seil FJ, editor. Advances in neurology, Vol 72. Neuronal regeneration, reorganization and repair. Philadelphia: Lippincott-Raven; 1997. p. 325-33.
14. Lawrence DG, Kuypers HGJM. The functional organization of the motor system in the monkey. Brain 1968;91:15-41.
15. Harris RM, Little JW, Goldstein B. Spared descending pathways mediate locomotor recovery after subtotal spinal cord injury. Neurosci Lett 1994;180:37-40.
16. Jane JA, Evans JP, Fisher LE. An investigation concerning the restitution of motor function following injury to the spinal cord. J Neurosurg 1964;21:167-71.
17. Kato M, Murakami S, Hirayama H, Hiking K. Recovery of postural control following chronic bilateral hemisection at different spinal cord levels in adult cat. Exp Neurol 1985;90:350-64.
18. Little JW. Recovery of function following spinal cord lesions in cats [dissertation]. Chicago (IL): University of Chicago; 1976.
19. Aoki M, Fujimoto Y, Kosaka I, Satomi H. Does collateral sprouting from corticospinal fibers participate in motor recovery after spinal hemisection in monkeys? In: Flohr H, editor. Post-lesion neuroplasticity. Berlin: Springer Verlag; 1988. p. 223-31.
20. Windle WF, Smart JO, Beers JJ. Residual function after subtotal spinal cord transection in adult cats. Neurology 1958;8:518-21.
21. Blight AR, DeCrescito V. Morphometric analysis of experimental spinal cord injury in the cat: the relation of injury intensity to survival of myelinated axons. Neuroscience 1986;19:321-41.
22. Eidelberg E, Walden JG, Nguyen LH. Locomotor control in macaque monkeys. Brain 1981;104:647-66.
23. Kaelan C, Jacobsen P, Morling P, Kakulas BA. A quantitative study of motoneurons and corticospinal fibres related to function in human spinal cord injury. Paraplegia 1989;27:148.
24. Peacock WJ, Shrosbree RD, Key AG. A review of 450 stab wounds of the spinal cord. S Afr Med J 1977;51:961-64.
25. Kakulas BA. Pathomorphological evidence for residual spinal cord functions. In: Eccles JC, Dimitrijevic MR, editors. Upper motor neuron function and dysfunction. Basel: Karger; 1985. p. 63-9.
26. Davies S, Illis LS, Raisman G. Regeneration in the central nervous system and related factors. Summary of the Bermuda Paraplegia Conference, April 1994. Paraplegia 1995;33:10-7.
27. Alexeeva N, Broton JG, Suys S, Calancie B. Central cord syndrome of cervical spinal cord injury: widespread changes in muscle recruitment studied by voluntary contractions and transcranial magnetic stimulation. Exp Neurol 1997;148:399-406.
28. Cadilhac J, Georgesco M, Benezech J, Duday H, Dapres G. Potential evoque cerebral somesthesique et reflexe d'Hoffmann dans les lesions medullaires aigues interet physiopathologique et pronostic. Electroencephalogr Clin Neurophysiol 1977;43:160-7.
29. Leis AA, Kronenberg MF, Stetkarova I, Paske WC, Stokic DS. Spinal motoneuron excitability following acute spinal cord injury in man. Neurology 1996;47:231-7.
30. Ko HY, Graziani V, Herbison GJ, Flanders AE, Ditunno JF. The pattern of reflex recovery during spinal shock [abstract]. J Spinal Cord Med 1997;20:143.
31. Nathan PW. Effects on movement of surgical incisions into the human spinal cord. Brain 1994;117:337-46.
32. Taylor RG, Gleave J. Incomplete spinal cord injuries with Brown-Séquard phenomena. J Bone Joint Surg 1957;39B: 438-50.
33. Holdsworth F. Fractures, dislocations, and fracture-dislocations of the spine. J Bone Joint Surg 1970;52A:1534-51.
34. Maynard FM, Reynolds GG, Fountain S, Wilmot C, Hamilton R. Neurological prognosis after traumatic quadriplegia. J Neurosurg 1979;50:611-6.
35. Brown PJ, Marino RJ, Herbison GJ, Ditunno JF Jr. The 72-hour examination as a predictor of recovery in in motor complete quadriplegia. Arch Phys Med Rehabil 1991;72:546-8.
36. Herbison GJ, Zerby SA, Cohen ME, Marino RJ, Ditunno JF. Motor power differences within the first two weeks post-SCI in cervical cord-injured quadriplegic subjects. J Neurotrauma 1992; 9:373-80.
37. Del Bigio MR, Johnson GE. Clinical presentation of spinal cord concussion. Spine 1989;14:37-40.
38. Little JW, Halar EM. H-reflex changes following spinal cord injury. Arch Phys Med Rehabil 1985;66:19-22.
39. Riddoch G. The reflex functions of the completely divided spinal cord in man, compared with those associated with less severe lesions. Brain 1917;40:264-402.
40. Kuhn RA, Macht MB. Some manifestations of reflex activity in man with particular reference to the occurrence of extensor spasm. Bull Johns Hopk Hosp 1949;84:43-75.
41. Little JW. Serial recording of reflexes after feline spinal cord transection. Exp Neurol 1986;93:510-21.
42. Nelson SG, Collatos TC, Niechaj A, Mendell LM. Immediate increase in Ia-motoneuron synaptic transmission caudal to spinal cord transection. J Neurophysiol 1979;42:655-64.
43. Malmsten J. Time course of segmental reflex changes after chronic cord hemisection in the rat. Acta Physiol Scand 1983;119: 435-43.
44. Murray JG, Thompson JW. Collateral sprouting in response to injury of the autonomic nervous system, and its consequences. BMJ 1957;13:213-9.
45. Twitchell TE. The restoration of motor function following hemiplegia in man. Brain 1951;74:443-80.
46. Barnes CD, Schadt JC. Release of function in the spinal cord. Prog Neurobiol 1979;12:1-13.
47. Jacobs BL, Fornal CA. 5-HT and motor control: a hypothesis. Trends Neurosci 1993;16:346-52.
48. Rymer WZ. Spinal cord injury: physiology and transplantation. In: Seil FJ, editor. Advances in neurology, Vol 59. New York: Raven Press Ltd; 1993. p. 157-62.
49. Illis LS. The motor neuron surface and spinal shock. Modern Trends Neurol 1967;4:53-68.
50. Rymer WZ, Powers RK. Conspectus: muscular weakness in incomplete spinal cord injury. Compr Ther 1987;13:3-7.
51. Klein WL, Sullivan J, Skorupa A, Aguilar JS. Plasticity of neuronal receptors. FASEB J 1989;3:2132-40.
52. Benson DM, Blitzer RD, Haroutunian V, Landau EM. Functional muscarinic supersensitivity in denervated rat hippocampus. Brain Res 1989;478:399-402.
53. Trugman JM, James CL. Rapid development of dopaminergic supersensitivity in reserpine-treated rats demonstrated with 14C-2-deoxyglucose autoradiography. J Neurosci 1992;12:2875-9.
54. Massari VJ, Shults CW, Park CW, Tizabi Y, Moody TW, Chronwall BM, et al. Deafferentation causes a loss of presynaptic bombesin receptors and supersensitivity of SP receptors in dorsal horn of cat. Brain Res 1985;343:268-74.
55. Ulas J, Monaghan DT, Cotman CW. Plastic response of hippocampal excitatory amino acid receptors to deafferentation and reinnervation. Neurosci 1990;34:9-17.
56. Biswas B, Jonsson G. Reversal of noradrenaline denervation-induced increase in beta-adrenoreceptor binding in rat neocortex by noradrenaline infusion. Eur J Pharmacol 1981;69:341-6.
57. Brown LM, Smith DL, Williams GM, Smith DJ. Alterations in serotonin binding sites after 5,7-dihydroxytryptamine treatment in the rat spinal cord. Neurosci Lett 1989;102:103-7.
58. Vita G, Haun CK, Hawkins EF, Engel WK. Autoradiographic localization of substance P receptors in rat spinal cord: effects of spinal transection. Funct Neurol 1987;2:421-6.
59. Roudet C, Savasta M, Feuerstein C. Normal distribution of alpha-1-adrenoceptors in the rat spinal cord and its modification after noradrenergic denervation: a quantitative autoradiography study. J Neurosci Res 1993;34:44-53.
60. Sawynok J, Reid A. Spinal supersensitivity to 5-HT1, 5HT2 and 5HT3 receptor agonists following 5,7 dihydroxytryptamine. Eur J Pharmacol 1994;264:249-57.
61. Bach-y-Rita P, Illis LS. Spinal shock: possible role of receptor plasticity and nonsynaptic transmission. Paraplegia 1993;31: 82-7.
62. DeKeyser J, Ebinger G, Vanquelin G. Evidence for a widespread dopaminergic innervation of the human cerebral cortex. Neurosci Lett 1989;104:281-5.
63. Shaw CA, Lanius RA. The origin of synaptic neuroplasticity: crucial molecules or a dynamical cascade? Brain Res Rev 1994;19:241-63.
64. Kroin JS, Bianchi GD, Penn RD. Spinal cord transection produces long-term increase in GABAB binding in the substantia gelatinosa. Synapse 1993;14:263-7.
65. Wall PD. Recruitment of ineffective synapses after injury. In: Seil FJ, editor. Advances in neurology, Vol 72. Neuronal regeneration, reorganization and repair. Philadelphia: Lippincott-Raven; 1997. p. 387-400.
66. Feldman MH. The decerebrate state in the primate. Arch Neurol 1971;25:501-16.
67. Steward O. Reorganization of neuronal connections following CNS trauma: principles and experimental paradigms. J Neurotrauma 1989;6:99-152.
68. Mendell LM. Physiological aspects of synaptic plasticity: the Ia/motoneuron connection as a model. In: Waxman SG, editor. Advances in neurology, Vol 47. Functional recovery in neurological disease. New York: Raven Press; 1988. p. 337-60.
69. Tatagiba M, Brosamle C, Schwab ME. Regeneration of injured axons in the adult mammalian central nervous system. Neurosurgery 1997;40:541-6.
70. Burke D. Spasticity as an adaptation to pyramidal tract injury. In: Waxman, SG, editor. Advances in neurology, Vol 47. Functional recovery in neurological disease. New York: Raven Press; 1988. p. 401-23.
71. Calancie B, Lutton S, Broton JG. Central nervous system plasticity after spinal cord injury in man: interlimb reflexes and the influence of cutaneous stimulation. Electroencephalogr Clin Neurophysiol 1996;101:304-15.
72. Nelson SG, Mendell LM. Enhancement in Ia-motoneuron synaptic transmission caudal to chronic spinal cord transaction. J Neurophysiol 1979;42:642-54.
73. Naciemiento W, Sappok T, Brook GA, Toth L, Schon SW, Noth J, et al. Structural changes of anterior horn neurons and their synaptic input caudal to a low thoracic spinal cord hemisection in the adult rat: a light and electron microscopic study. Acta Neuropathol 1995;30:552-64.
74. McBride WJ, Shapiro S, Chernet E, Sartorius C, Hall PV. Effects of dorsal bilateral rhizotomy treatment on transmitter systems in the spinal cord of normal and spastic dogs. J Neurochem 1988;50:603-8.
75. Marty S, Berzaghi MP, Berninger B. Neurotrophins and activity-dependent plasticity of cortical interneurons. Trends Neurosci 1997;20:198-202.
76. Goldberger ME. The use of behavioral methods to predict spinal cord plasticity. Restor Neurol Neurosci 1991;2:339-50.
77. Bullitt E, Stofer WD, Vierck CJ, Perl ER. Reorganization of primary afferent nerve terminals in the spinal dorsal horn of the primate caudal to anterolateral chordotomy. J Comp Neurol 1988;270:549-58.
78. de Groat WC. Mechanisms underlying the recovery of lower urinary tract function following spinal cord injury. Paraplegia 1995;33:493-505.
79. Pullen AH, Sears TA. Modification of 'C' synapses following partial central deafferentation of thoracic motoneurones. Brain Res 1978;145:141-6.
80. Goldstein B, Little JW, Harris RM. Axonal sprouting following incomplete spinal cord injury: an experimental model. J Spinal Cord Med 1997;20:200-6.
81. Krassioukov AV, Weaver LC. Morphological changes in sympathetic preganglionic neurons after spinal cord injury in rats. Neurosci 1996;70:211-25.
82. Benowitz LI, Routtenberg A. GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 1997;20: 84-91.
83. Sperry MA, Goshgarian HG. Ultrastructural changes in the rat phrenic nucleus developing within 2 h after cervical spinal cord hemisection. Exp Neurol 1993;120:233-44.
84. Brenowitz GL. Time-course for receptive field plasticity following spinal cord hemisection. Brain Res 1983;279:250-3.
85. McCouch GP, Austin GM, Liu CN, Liu CY. Sprouting as a cause of spasticity. J Neurophysiol 1958;21:205-16.
86. Munson JB, Foehring RC, Lofton SA, Zengel JE, Sypert GW. Plasticity of medial gastrocnemius motor units following cordotomy in the cat. J Neurophysiol 1986;55:619-34.
87. Hochman S, McCrea DA. Effects of chronic spinalization on ankle extensor motoneurons. I. Composite monosynaptic Ia EPSPs in four motoneuron pools. J Neurophysiol 1994;71: 1452-67.
88. Hultborn H, Malmsten J. Changes in segmental reflexes following chronic spinal cord hemisection in the cat. II. Conditioned monosynaptic test reflexes. Acta Physiol Scand 1983;119:423-33.
89. Thompson RF, Reier PJ, Lucas CC, Parmer R. Altered patterns of reflex excitability subsequent to contusion injury of the rat spinal cord. J Neurophysiol 1992;68:1473-86.
90. Aoki M, Mori S, Fujimori B. Exaggeration of knee-jerk following spinal hemisection in monkeys. Brain Res 1976;197:471-85.
91. Goldfarb J. Excitation of Renshaw cells via motor neuron collaterals in acute and chronic spinal cats. Brain Res 1976;106: 176-83.
92. Nacimiento W, Mautes A, Topper R, Oestreicher AB, Gispen WH, Nacimiento AC, et al. B-50 (GAP-43) in the spinal cord caudal to hemisection: indication for lack of intraspinal sprouting in dorsal root axons. J Neurosci Res 1993;35:603-17.
93. Rodin BE, Sampogna SL, Kruger L. An examination of intraspinal sprouting in dorsal root axons with the tracer horseradish peroxidase. J Comp Neurol 1983;215:187-98.
94. Little JW, Harris RM, Lerner SJ. Immobilization impairs recovery after spinal cord injury. Arch Phys Med Rehabil 1991;72: 408-12.
95. Muir GD, Sleeves JD. Sensorimotor stimulation to improve locomotor recovery after spinal cord injury. Trends Neurosci 1997;20:72-7.
96. Barbeau H, Rossignol S. Recovery of locomotion after chronic spinalization in the adult cat. Brain Res 1987;412:84-95.
97. Dietz V, Wirz M, Jensen L. Locomotion in patients with spinal cord injuries. Phys Ther 1997;77:508-16.
98. Burgess JW, Villablanca JR. Recovery of function after neonatal or adult hemispherectomy in cats. II. Limb bias and development, paw usage, locomotion and rehabilitative effects of exercise. Behav Brain Res 1986;20:1-18.
99. Yu J. Functional recovery with and without training following brain damage in experimental animals: a review. Arch Phys Med Rehabil 1976;57:38-41.
100. Nudo RJ, Wise BM, SiFuentes F, Milliken GW. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 1996;21:1791-94.
101. Yu J, Liu CN, Chambers WW, Chen WP, McCouch GP. Effects of exercise on reflexes in paraplegic monkeys. Acta Neurobiol Exp (Warsz) 1981;41:271-7.
102. Guttmann L. Studies on reflex activity of the isolated spinal cord in spinal man. J Nerv Ment Dis 1952;116:957-72.
103. Nathan PW. Factors affecting spasticity. Int Rehabil Med 1980;2: 27-30.
104. Little JW, Harris RM, Smithson D. Motor recovery in the absence of segmentai afferents: a case study of incomplete spinal cord injury. Paraplegia 1989;27:385-9.
105. Maynard FM, Karunas RS, Waring WP. Epidemiology of spasticity following traumatic spinal cord injury. Arch Phys Med Rehabil 1990;71:566-9.
106. Little JW, Micklesen P, Umlauf R, Britell C. Lower extremity manifestations of spasticity in chronic spinal cord injury. Am J Phys Med Rehabil 1989;68:32-6.
107. Brady ST. Axonal dynamics and regeneration. In: Gorio A, editor. Neuroregeneration. New York: Raven Press Ltd; 1993. p. 7-36.
108. Futerman AH, Banker GA. The economics of neunte outgrowth - the addition of new membrane to growing axons. Trends Neurosci 1996;19:144-9.
109. Steward O. Signals that induce sprouting in the central nervous system: sprouting is delayed in a strain of mice exhibiting delayed axonal degeneration. Exp Neurol 1992;118:340-51.
110. Brown TH, Kairiss EW, Keenan CL. Hebbian synapses: biophysical mechanisms and algorithms. Annu Rev Neurosci 1990;13:475-511.
111. Cotman CW, Neeper S. Activity-dependent plasticity and the aging brain. In: Schneider EL, Rowe JW. Handbook of the biology of aging. 4th ed. New York: Academic Press; 1996. p. 283-95.
112. Pfrieger FW, Barres BA. New views on synapse-glia interactions. Curr Opin Neurobiol 1996;6:615-21.
113. Field PM, Coldham DE, Raisman O. Synapse formation after injury in the adult rat brain: preferential reinnervation of denervated fimbrial sites by axons of the contralateral fimbria. Brain Res 1980;189:103-13.
114. Lichtman JW, Balice-Gordon RJ. Understanding synaptic competition in theory and in practice. J Neurobiol 1990;21:99-106.
115. Snider WD, Lichtman JW. Are neurotrophins synaptotrophins? Mol Cell Neurosci 1996;7:433-42.
116. Wernig A, Muller S. Laufband locomotion with body weight support improved walking in persons with severe spinal cord injuries. Paraplegia 1992;30:229-38.
117. Walker-Batson D, Smith P, Curtis S, Unwin H, Greenlee R. Amphetamine paired with physical therapy accelerates motor recovery after stroke. Stroke 1995;26:2254-59.
118. Schallert T, Jones TA. "Exuberant" neuronal growth after brain damage in adult rats: the essential role of behavioral experience. J Neurol Transpl Plastic 1993;4:193-8.
119. Black P, Markowitz RS, Cianci SN. Recovery of motor function after lesions in motor cortex in monkey. In: CIBA Foundation, editor. Outcome of severe damage to the central nervous system. Amsterdam: Elsevier; 1975. p. 65-83.