Human spinal cord injury: Motor unit properties and behaviour

Acta Physiologica

Volumn 210, Issue 1, 2014, Pages 5-19

  Thomas, C K ^a   Bakels, R ^b   Klein, C S ^c   Zijdewind, I ^b  

^a UNIVERSITY OF MIAMI   (United States)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c REHABILITATION INSTITUTE OF CHICAGO   (United States)

Author keywords

Axon conduction velocity; Maximal voluntary force; Motor unit firing frequency; Motor unit recruitment; Muscle spasms

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; BACLOFEN; CHLORPROMAZINE; CYPROHEPTADINE; ZOLMITRIPTAN;

AFTERHYPERPOLARIZATION; BEHAVIOR; BLADDER FUNCTION; BRAIN COMPUTER INTERFACE; DENERVATION; ELECTROMYOGRAPHY; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FLEXOR MUSCLE; FUNCTIONAL ELECTRICAL STIMULATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAND FUNCTION; HAND MUSCLE; HOFFMANN REFLEX; HUMAN; INTERNEURON; INTESTINE FUNCTION; LOCOMOTION; MOTONEURON; MOTOR UNIT; MUSCLE ACTION POTENTIAL; MUSCLE ATROPHY; MUSCLE FATIGUE; MUSCLE INNERVATION; MUSCLE REFLEX; MUSCLE SPASM; MUSCLE STRENGTH; MUSCLE TWITCH; MUSCLE WEAKNESS; NERVE CELL NECROSIS; NERVE CONDUCTION; NERVE EXCITABILITY; NERVE FIBER; NERVE FIBER MEMBRANE; NEUROPHYSIOLOGICAL RECRUITMENT; NONHUMAN; PARALYSIS; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; PYRAMIDAL TRACT; REVIEW; SEXUAL FUNCTION; SPINAL CORD INJURY; SPINAL CORD MOTONEURON; SPINAL CORD NERVE CELL; SPINAL CORD TRANSSECTION; TETANY; TRANSCRANIAL MAGNETIC STIMULATION; VENTRAL ROOT;

AXON CONDUCTION VELOCITY; MAXIMAL VOLUNTARY FORCE; MOTOR UNIT FIRING FREQUENCY; MOTOR UNIT RECRUITMENT; MUSCLE SPASMS;

ANIMALS; HUMANS; MODELS, NEUROLOGICAL; MOTOR NEURONS; MOVEMENT; MUSCLE CONTRACTION; MUSCLE, SKELETAL; NEURAL CONDUCTION; NEUROMUSCULAR JUNCTION; SPINAL CORD; SPINAL CORD INJURIES; SYNAPTIC TRANSMISSION;

EID: 84890197689     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12153     Document Type: Review

References (150)

1. Anderson, K.D. 2004. Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma 21, 1371-1383.
2. Bakels, R. & Kernell, D. 1993. Matching between motoneurone and muscle unit properties in rat medial gastrocnemius. J Physiol (Lond) 463, 307-324.
3. Bakels, R. & Kernell, D. 1994. Threshold-spacing in motoneurone pools of rat and cat: possible relevance for manner of force gradation. Exp Brain Res 102, 69-74.
4. Bawa, P. & Murnaghan, C. 2009. Motor unit rotation in a variety of human muscles. J Neurophysiol 102, 2265-2272.
5. Beaumont, E., Houle, J.D., Peterson, C.A. & Gardiner, P.F. 2004. Passive exercise and fetal spinal cord transplant both help to restore motoneuronal properties after spinal cord transection in rats. Muscle Nerve 29, 234-242.
6. Bennett, K.M. & Lemon, R.N. 1994. The influence of single monkey cortico-motoneuronal cells at different levels of activity in target muscles. J Physiol (Lond) 477, 291-307.
7. Bennett, D.J., Li, Y., Harvey, P.J. & Gorassini, M. 2001. Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. J Neurophysiol 86, 1972-1982.
8. Bhadra, N. & Kilgore, K.L. 2004. Direct current electrical conduction block of peripheral nerve. IEEE Trans Neural Syst Rehabil Eng 12, 313-324.
9. Bigland-Ritchie, B., Fuglevand, A.J. & Thomas, C.K. 1998. Contractile properties of human motor units: is man a cat? The Neuroscientist 4, 240-249.
10. Binder, M.D., Heckman, C.J. & Powers, R.K. 1996. The physiological control of motoneuron activity. In: L.B. Rowell & J.T. Shepherd (eds) Handbook of Physiology. Section 12, Exercise: Regulation and Integration of Multiple Systems, pp. 3-53. Oxford, New York.
11. Boland, R.A., Lin, C.S., Engel, S. & Kiernan, M.C. 2011. Adaptation of motor function after spinal cord injury: novel insights into spinal shock. Brain 134, 495-505.
12. Boulenguez, P., Liabeuf, S., Bos, R., Bras, H., Jean-Xavier, C., Brocard, C., Stil, A., Darbon, P., Cattaert, D., Delpire, E., Marsala, M. & Vinay, L. 2010. Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat Med 16, 302-307.
13. Brouwer, B., Bugaresti, J. & Ashby, P. 1992. Changes in corticospinal facilitation of lower limb spinal motor neurons after spinal cord lesions. J Neurol Neurosurg Psychiatry 55, 20-24.
14. Bryden, A.M., Kilgore, K.L., Lind, B.B. & Yu, D.T. 2004. Triceps denervation as a predictor of elbow flexion contractures in C5 and C6 tetraplegia. Arch Phys Med Rehabil 85, 1880-1885.
15. Bunge, R.P., Puckett, W.R., Becerra, J.L., Marcillo, A. & Quencer, R.M. 1993. Observations on the pathology of human spinal cord injury. A review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. Adv Neurol 59, 75-89.
16. Burke, R.E. 1967. Motor unit types of cat triceps surae muscle. J Physiol (Lond) 193, 141-160.
17. Button, D.C., Kalmar, J.M., Gardiner, K., Marqueste, T., Zhong, H., Roy, R.R., Edgerton, V.R. & Gardiner, P.F. 2008. Does elimination of afferent input modify the changes in rat motoneurone properties that occur following chronic spinal cord transection? J Physiol (Lond) 586, 529-544.
18. Calancie, B., Broton, J.G., Klose, K.J., Traad, M., Difini, J. & Ayyar, D.R. 1993. Evidence that alterations in presynaptic inhibition contribute to segmental hypo- and hyperexcitability after spinal cord injury in man. Electroencephalogr Clin Neurophysiol 89, 177-186.
19. Calancie, B., Needham-Shropshire, B., Jacobs, P., Willer, K., Zych, G. & Green, B.A. 1994. Involuntary stepping after chronic spinal cord injury. Evidence for a central rhythm generator for locomotion in man. Brain 117, 1143-1159.
20. Calancie, B., Molano, M.R. & Broton, J.G. 2002. Interlimb reflexes and synaptic plasticity become evident months after human spinal cord injury. Brain 125, 1150-1161.
21. Calancie, B., Alexeeva, N., Broton, J.G. & Molano, M.R. 2005. Interlimb reflex activity after spinal cord injury in man: strengthening response patterns are consistent with ongoing synaptic plasticity. Clin Neurophysiol 116, 75-86.
22. Celichowski, J., Mrowczynski, W., Krutki, P., Gorska, T., Majczynski, H. & Slawinska, U. 2006. Changes in contractile properties of motor units of the rat medial gastrocnemius muscle after spinal cord transection. Exp Physiol 91, 887-895.
23. Celichowski, J., Krysciak, K., Krutki, P., Majczynski, H., Gorska, T. & Slawinska, U. 2010. Time-related changes of motor unit properties in the rat medial gastrocnemius muscle after the spinal cord injury. II. Effects of a spinal cord hemisection. J Electromyogr Kinesiol 20, 532-541.
24. Cope, T.C., Bodine, S.C., Fournier, M. & Edgerton, V.R. 1986. Soleus motor units in chronic spinal transected cats: physiological and morphological alterations. J Neurophysiol 55, 1202-1220.
25. Courtine, G., Gerasimenko, Y., van den Brand, R., Yew, A., Musienko, P., Zhong, H., Song, B., Ao, Y., Ichiyama, R.M., Lavrov, I., Roy, R.R., Sofroniew, M.V. & Edgerton, V.R. 2009. Transformation of nonfunctional spinal circuits into functional states after the loss of brain input. Nat Neurosci 12, 1333-1342.
26. D'Amico, J.M., Li, Y., Bennett, D.J. & Gorassini, M.A. 2013a. Reduction of spinal sensory transmission by facilitation of 5-HT1B/D receptors in noninjured and spinal cord-injured humans. J Neurophysiol 109, 1485-1493.
27. D'Amico, J.M., Murray, K.C., Li, Y., Chan, K.M., Finlay, M.G., Bennett, D.J. & Gorassini, M.A. 2013b. Constitutively active 5-HT2/α1 receptors facilitate muscle spasms after human spinal cord injury. J Neurophysiol 109, 1473-1484.
28. Davey, N.J., Ellaway, P.H., Friedland, C.L. & Short, D.J. 1990. Motor unit discharge characteristics and short term synchrony in paraplegic humans. J Neurol Neurosurg Psychiatry 53, 764-769.
29. Davey, N.J., Smith, H.C., Wells, E., Maskill, D.W., Savic, G., Ellaway, P.H. & Frankel, H.L. 1998. Responses of thenar muscles to transcranial magnetic stimulation of the motor cortex in patients with incomplete spinal cord injury. J Neurol Neurosurg Psychiatry 65, 80-87.
30. De Luca, C.J., LeFever, R.S., McCue, M.P. & Xenakis, A.P. 1982. Behaviour of human motor units in different muscles during linearly varying contractions. J Physiol (Lond) 329, 113-128.
31. Dengler, R., Stein, R.B. & Thomas, C.K. 1988. Axonal conduction velocity and force of single human motor units. Muscle Nerve 11, 136-145.
32. Enoka, R.M. & Fuglevand, A.J. 2001. Motor unit physiology: some unresolved issues. Muscle Nerve 24, 4-17.
33. Fleshman, J.W., Munson, J.B., Sypert, G.W. & Friedman, W.A. 1981. Rheobase, input resistance, and motor-unit type in medial gastrocnemius motoneurons in the cat. J Neurophysiol 46, 1326-1338.
34. Gallego, R., Huizar, P., Kudo, N. & Kuno, M. 1978. Disparity of motoneurone and muscle differentiation following spinal transection in the kitten. J Physiol (Lond) 281, 253-265.
35. Gardiner, P.F. & Kernell, D. 1990. The "fastness" of rat motoneurones: time-course of afterhyperpolarization in relation to axonal conduction velocity and muscle unit contractile speed. Pflugers Arch 415, 762-766.
36. Geisler, F.H., Coleman, W.P., Grieco, G. & Poonian, D. & Sygen Study Group. 2001. The Sygen multicenter acute spinal cord injury study. Spine (Phila Pa 1976) 26, S87-S98.
37. Georgopoulos, A.P., Schwartz, A.B. & Kettner, R.E. 1986. Neuronal population coding of movement direction. Science 233, 1416-1419.
38. Gonzalez, H., Olsson, T. & Borg, K. 2010. Management of postpolio syndrome. Lancet Neurol 9, 634-642.
39. Gorassini, M.A., Bennett, D.J. & Yang, J.F. 1998. Self-sustained firing of human motor units. Neurosci Lett 247, 13-16.
40. Gorassini, M.A., Knash, M.E., Harvey, P.J., Bennett, D.J. & Yang, J.F. 2004. Role of motoneurons in the generation of muscle spasms after spinal cord injury. Brain 127, 2247-2258.
41. Gordon, T., Tyreman, N., Rafuse, V.F. & Munson, J.B. 1997. Fast-to-slow conversion following chronic low-frequency activation of medial gastrocnemius muscle in cats. I. Muscle and motor unit properties. J Neurophysiol 77, 2585-2604.
42. Gossen, E.R., Ivanova, T. & Garland, S.J. 2003. The time course of the motoneurone afterhyperpolarization is related to motor unit twitch speed in human skeletal muscle. J Physiol (Lond) 552, 657-664.
43. Grande, G., Bui, T.V. & Rose, P.K. 2007. Effect of localized innervation of the dendritic trees of feline motoneurons on the amplification of synaptic input: a computational study. J Physiol (Lond) 583, 611-630.
44. Grande, G., Bui, T.V. & Rose, P.K. 2010. Distribution of vestibulospinal contacts on the dendrites of ipsilateral splenius motoneurons: an anatomical substrate for push-pull interactions during vestibulocollic reflexes. Brain Res 1333, 9-27.
45. Griffin, L., Godfrey, S. & Thomas, C.K. 2002. Stimulation pattern that maximizes force in paralyzed and control whole thenar muscles. J Neurophysiol 87, 2271-2278.
46. Grumbles, R.M., Brunschwig, J. & Thomas, C.K. 1999. Motoneuron death after spinal cord injury. J Neurotrauma 16, 997.
47. Guest, J.D., Hiester, E.D. & Bunge, R.P. 2005. Demyelination and Schwann cell responses adjacent to injury epicenter cavities following chronic human spinal cord injury. Exp Neurol 192, 384-393.
48. Gydikov, A. & Kosarov, D. 1974. Some features of different motor units in human biceps brachii. Pflugers Arch 347, 75-88.
49. Häger-Ross, C.K., Klein, C.S. & Thomas, C.K. 2006. Twitch and tetanic properties of human thenar motor units paralyzed by chronic spinal cord injury. J Neurophysiol 96, 165-174.
50. Havton, L.A., Hotson, J.R. & Kellerth, J.O. 2001. Partial peripheral motor nerve lesions induce changes in the conduction properties of remaining intact motoneurons. Muscle Nerve 24, 662-666.
51. Heckmann, C.J., Gorassini, M.A. & Bennett, D.J. 2005. Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle Nerve 31, 135-156.
52. Hensbergen, E. & Kernell, D. 1997. Daily durations of spontaneous activity in cat's ankle muscles. Exp Brain Res 115, 325-332.
53. Hochman, S. & McCrea, D.A. 1994. Effects of chronic spinalization on ankle extensor motoneurons II. Motoneuron electrical properties. J Neurophysiol 71, 1468-1479.
54. Huizar, P., Kuno, M. & Miyata, Y. 1975. Differentiation of motoneurones and skeletal muscles in kittens. J Physiol (Lond) 252, 465-479.
55. Huizar, P., Kuno, M., Kudo, N. & Miyata, Y. 1977. Reaction of intact spinal motoneurones to partial denervation of the muscle. J Physiol (Lond) 265, 175-191.
56. James, N.D., Bartus, K., Grist, J., Bennett, D.L., McMahon, S.B. & Bradbury, E.J. 2011. Conduction failure following spinal cord injury: functional and anatomical changes from acute to chronic stages. J Neurosci 31, 18543-18555.
57. Janssen, T.W., Bakker, M., Wyngaert, A., Gerrits, K.H. & de Haan, A. 2004. Effects of stimulation pattern on electrical stimulation-induced leg cycling performance. J Rehabil Res Dev 41, 787-796.
58. Kakei, S., Hoffman, D.S. & Strick, P.L. 1999. Muscle and movement representations in the primary motor cortex. Science 285, 2136-2139.
59. Keen, D.A., Chou, L.W., Nordstrom, M.A. & Fuglevand, A.J. 2012. Short-term synchrony in diverse motor nuclei presumed to receive different extents of direct cortical input. J Neurophysiol 108, 3264-3275.
60. Kern, D.S., Semmler, J.G. & Enoka, R.M. 2001. Long-term activity in upper- and lower-limb muscles of humans. J Appl Physiol 91, 2224-2232.
61. Kern, H., Boncompagni, S., Rossini, K., Mayr, W., Fano, G., Zanin, M.E., Podhorska-Okolow, M., Protasi, F. & Carraro, U. 2004. Long-term denervation in humans causes degeneration of both contractile and excitation-contraction coupling apparatus, which is reversible by functional electrical stimulation (FES): a role for myofiber regeneration? J Neuropathol Exp Neurol 63, 919-931.
62. Kernell, D. 1965. The limits of firing frequency in cat lumbosacral motoneurones possessing different time course of afterhyperpolarization. Acta Physiol Scand 65, 87-100.
63. Kernell, D. 1998. Muscle regionalization. Can J Appl Physiol 23, 1-22.
64. Kernell, D. 2006. The Motoneurone and its Muscle Fibres. Oxford University Press, Oxford.
65. Kernell, D. & Hultborn, H. 1990. Synaptic effects on recruitment gain: a mechanism of importance for the input-output relations of motoneurone pools? Brain Res 507, 176-179.
66. Kernell, D., Eerbeek, O., Verhey, B.A. & Donselaar, Y. 1987. Effects of physiological amounts of high- and low-rate chronic stimulation on fast-twitch muscle of the cat hindlimb. I. Speed- and force-related properties. J Neurophysiol 58, 598-613.
67. Kiehn, O. & Eken, T. 1997. Prolonged firing in motor units: evidence of plateau potentials in human motoneurons? J Neurophysiol 78, 3061-3068.
68. Klein, C.S., Häger-Ross, C.K. & Thomas, C.K. 2006. Fatigue properties of human thenar motor units paralysed by chronic spinal cord injury. J Physiol (Lond) 573, 161-171.
69. Klein, C.S., Peterson, L.B., Ferrell, S. & Thomas, C.K. 2010. Sensitivity of 24-h EMG duration and intensity in the human vastus lateralis muscle to threshold changes. J Appl Physiol 108, 655-661.
70. Kokotilo, K.J., Eng, J.J. & Curt, A. 2009. Reorganization and preservation of motor control of the brain in spinal cord injury: a systematic review. J Neurotrauma 25, 2113-2126.
71. Kukulka, C.G. & Clamann, H.P. 1981. Comparison of the recruitment and discharge properties of motor units in human brachial biceps and adductor pollicis during isometric contractions. Brain Res 219, 45-55.
72. Lemon, R.N. 2008. Descending pathways in motor control. Annu Rev Neurosci 31, 195-218.
73. Li, Y. & Bennett, D.J. 2003. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90, 857-869.
74. Li, Y., Gorassini, M.A. & Bennett, D.J. 2004a. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 91, 767-783.
75. Li, Y., Li, X., Harvey, P.J. & Bennett, D.J. 2004b. Effects of baclofen on spinal reflexes and persistent inward currents in motoneurons of chronic spinal rats with spasticity. J Neurophysiol 92, 2694-2703.
76. Lieberman, J.S., Corkill, G., Nayak, N.N., French, B.N. & Taylor, R.G. 1980. Serial phrenic nerve conduction studies in candidates for diaphragm pacing. Arch Phys Med Rehabil 61, 528-531.
77. Macefield, V.G., Gandevia, S.C., Bigland-Ritchie, B., Gorman, R.B. & Burke, D. 1993. The firing rates of human motoneurones voluntarily activated in the absence of muscle afferent feedback. J Physiol (Lond) 471, 429-443.
78. Manuel, M. & Heckman, C.J. 2011. Adult mouse motor units develop almost all of their force in the subprimary range: a new all-or-none strategy for force recruitment? J Neurosci 31, 15188-15194.
79. Marino, R.J., Herbison, G.J. & Ditunno, J.F. Jr 1994. Peripheral sprouting as a mechanism for recovery in the zone of injury in acute quadriplegia: a single-fiber EMG study. Muscle Nerve 17, 1466-1468.
80. Mayer, R.F., Burke, R.E., Toop, J., Walmsley, B. & Hodgson, J.A. 1984. The effect of spinal cord transection on motor units in cat medial gastrocnemius muscles. Muscle Nerve 7, 23-31.
81. McComas, A.J., Fawcett, P.R., Campbell, M.J. & Sica, R.E. 1971. Electrophysiological estimation of the number of motor units within a human muscle. J Neurol Neurosurg Psychiatry 34, 121-131.
82. McKay, W.B., Ovechkin, A.V., Vitaz, T.W., Terson de Paleville, D.G. & Harkema, S.J. 2011. Long-lasting involuntary motor activity after spinal cord injury. Spinal Cord 49, 87-93.
83. Monster, A.W. & Chan, H. 1977. Isometric force production by motor units of extensor digitorum communis muscle in man. J Neurophysiol 40, 1432-1443.
84. Moritz, C.T., Barry, B.K., Pascoe, M.A. & Enoka, R.M. 2005. Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. J Neurophysiol 93, 2449-2459.
85. Mrówczyński, W., Celichowski, J., Krutki, P., Górska, T., Majczyński, H. & Slawińska, U. 2010. Time-related changes of motor unit properties in the rat medial gastrocnemius muscle after spinal cord injury. I. Effects of total spinal cord transection. J Electromyogr Kinesiol 20, 523-531.
86. Mulcahey, M.J., Smith, B.T. & Betz, R.R. 1999. Evaluation of the lower motor neuron integrity of upper extremity muscles in high level spinal cord injury. Spinal Cord 37, 585-591.
87. Munson, J.B., Foehring, R.C., Lofton, S.A., Zengel, J.E. & Sypert, G.W. 1986. Plasticity of medial gastrocnemius motor units following cordotomy in the cat. J Neurophysiol 55, 619-634.
88. Murray, K.C., Nakae, A., Stephens, M.J., Rank, M., D'Amico, J., Harvey, P.J., Li, X., Harris, R.L., Ballou, E.W., Anelli, R. et al. 2010. Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors. Nat Med 16, 694-700.
89. Murray, K.C., Stephens, M.J., Rank, M., D'Amico, J., Gorassini, M.A. & Bennett, D.J. 2011. Polysynaptic excitatory postsynaptic potentials that trigger spasms after spinal cord injury in rats are inhibited by 5-HT1B and 5-HT1F receptors. J Neurophysiol 106, 925-943.
90. Needham-Shropshire, B.M., Klose, K.J., Tucker, M.E. & Thomas, C.K. 1997. Manual muscle test score and force comparisons after cervical spinal cord injury. J Spinal Cord Med 20, 324-330.
91. Nguyen, R., Masani, K., Micera, S., Morari, M. & Popovic, M.R. 2011. Spatially distributed sequential stimulation reduces fatigue in paralyzed triceps surae muscles: a case study. Artif Organs 35, 1174-1180.
92. Nogajski, J.H., Engel, S. & Kiernan, M.C. 2006. Focal and generalized peripheral nerve dysfunction in spinal cord-injured patients. J Clin Neurophysiol 23, 273-279.
93. Nollet, F. 2010. Postpolio syndrome: unanswered questions regarding cause, course, risk factors, and therapies. Lancet Neurol 9, 561-563.
94. Norton, J.A., Bennett, D.J., Knash, M.E., Murray, K.C. & Gorassini, M.A. 2008. Changes in sensory-evoked synaptic activation of motoneurons after spinal cord injury in man. Brain 131, 1478-1491.
95. Oudega, M. & Perez, M.A. 2012. Corticospinal reorganization after spinal cord injury. J Physiol (Lond) 590, 3647-3663.
96. Oya, T., Riek, S. & Cresswell, A.G. 2009. Recruitment and rate coding organisation for soleus motor units across entire range of voluntary isometric plantar flexions. J Physiol (Lond) 587, 4737-4748.
97. Peckham, P.H., Mortimer, J.T. & Marsolais, E.B. 1976a. Upper and lower motor neuron lesions in the upper extremity muscles of tetraplegics. Paraplegia 14, 115-121.
98. Peckham, P.H., Mortimer, J.T. & Marsolais, E.B. 1976b. Alteration in the force and fatigability of skeletal muscle in quadriplegic humans following exercise induced by chronic electrical stimulation. Clin Orthop Relat Res 114, 326-333.
99. Petersen, N.T., Taylor, J.L. & Gandevia, S.C. 2002. The effect of electrical stimulation of the corticospinal tract on motor units of the human biceps brachii. J Physiol (Lond) 544, 277-284.
100. Piotrkiewicz, M., Kudina, L., Hausmanowa-Petrusewicz, I., Zhoukovskaya, N. & Mierzejewska, J. 2001. Discharge properties and afterhyperpolarization of human motoneurons supplying slow and fast muscles. Biocybernetics and Biomedical Engineering 21, 53-75.
101. Powers, R.K., Elbasiouny, S.M., Rymer, W.Z. & Heckman, C.J. 2012. Contribution of intrinsic properties and synaptic inputs to motoneuron discharge patterns: a simulation study. J Neurophysiol 107, 808-823.
102. Rack, P.M. & Westbury, D.R. 1969. The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol (Lond) 204, 443-460.
103. Ragnarsson, K.T. 2008. Functional electrical stimulation after spinal cord injury: current use, therapeutic effects and future directions. Spinal Cord 46, 255-274.
104. Rank, M.M., Murray, K.C., Stephens, M.J., D'Amico, J., Gorassini, M.A. & Bennett, D.J. 2011. Adrenergic receptors modulate motoneuron excitability, sensory synaptic transmission and muscle spasms after chronic spinal cord injury. J Neurophysiol 105, 410-422.
105. Revill, A.L. & Fuglevand, A.J. 2011. Effects of persistent inward currents, accommodation, and adaptation on motor unit behavior: a simulation study. J Neurophysiol 106, 1467-1479.
106. Riley, D.A., Burns, A.S., Carrion-Jones, M. & Dillingham, T.R. 2011. Electrophysiological dysfunction in the peripheral nervous system following spinal cord injury. PM R 3, 419-425.
107. Robinson, G.A., Enoka, R.M. & Stuart, D.G. 1991. Immobilization-induced changes in motor unit force and fatigability in the cat. Muscle Nerve 14, 563-573.
108. 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. 2010. Extensive spontaneous plasticity of corticospinal projections after primate spinal cord injury. Nat Neurosci 13, 1505-1510.
109. Ryge, J., Winther, O., Wienecke, J., Sandelin, A., Westerdahl, A.C., Hultborn, H. & Kiehn, O. 2010. Transcriptional regulation of gene expression clusters in motor neurons following spinal cord injury. BMC Genomics 11, 365.
110. Sasaki, S., Isa, T., Pettersson, L.G., Alstermark, B., Naito, K., Yoshimura, K., Seki, K. & Ohki, Y. 2004. Dexterous finger movements in primate without monosynaptic corticomotoneuronal excitation. J Neurophysiol 92, 3142-3147.
111. Schindler-Ivens, S.M. & Shields, R.K. 2004. Soleus H-reflex recruitment is not altered in persons with chronic spinal cord injury. Arch Phys Med Rehabil 85, 840-847.
112. Scott, W.B., Lee, S.C., Johnston, T.E., Binkley, J. & Binder-Macleod, S.A. 2007. Effect of electrical stimulation pattern on the force responses of paralyzed human quadriceps muscles. Muscle Nerve 35, 471-478.
113. Shields, R.K. & Dudley-Javoroski, S. 2006. Musculoskeletal plasticity after acute spinal cord injury: effects of long-term neuromuscular electrical stimulation training. J Neurophysiol 95, 2380-2390.
114. Smith, H.C., Davey, N.J., Savic, G., Maskill, D.W., Ellaway, P.H. & Frankel, H.L. 1999. Motor unit discharge characteristics during voluntary contraction in patients with incomplete spinal cord injury. Exp Physiol 84, 1151-1160.
115. Smith, H.C., Davey, N.J., Savic, G., Maskill, D.W., Ellaway, P.H., Jamous, M.A. & Frankel, H.L. 2000. Modulation of single motor unit discharges using magnetic stimulation of the motor cortex in incomplete spinal cord injury. J Neurol Neurosurg Psychiatry 68, 516-520.
116. Steeves, J.D., Lammertse, D.P., Kramer, J.L., Kleitman, N., Kalsi-Ryan, S., Jones, L., Curt, A., Blight, A.R. & Anderson, K.D. 2012. Outcome measures for Acute/Subacute Cervical Sensorimotor Complete (AIS-A) spinal cord injury during a phase 2 clinical trial. Top Spinal Cord Inj Rehabil 18, 1-14.
117. Stein, R.B., Brucker, B.S. & Ayyar, D.R. 1990. Motor units in incomplete spinal cord injury: electrical activity, contractile properties and the effects of biofeedback. J Neurol Neurosurg Psychiatry 53, 880-885.
118. Stein, R.B., Gordon, T., Jefferson, J., Sharfenberger, A., Yang, J.F., de Zepetnek, J.T. & Belanger, M. 1992. Optimal stimulation of paralyzed muscle after human spinal cord injury. J Appl Physiol 72, 1393-1400.
119. Thomas, C.K. 1995. Human motor units studied by spike-triggered averaging and intraneural motor axon stimulation. Adv Exp Med Biol 384, 147-160.
120. Thomas, C.K. 1997a. Contractile properties of human thenar muscles paralyzed by spinal cord injury. Muscle Nerve 20, 788-799.
121. Thomas, C.K. 1997b. Fatigue in human thenar muscles paralysed by spinal cord injury. J Electromyogr Kinesiol 7, 15-26.
122. Thomas, C.K. & del Valle, A. 2001. The role of motor unit rate modulation versus recruitment in repeated submaximal voluntary contractions performed by control and spinal cord injured subjects. J Electromyogr Kinesiol 11, 217-229.
123. Thomas, C.K. & Kozhina, G. 1999. Motor unit firing rates during voluntary contractions. XVIIth Congress of the international Society of Biomechanics, Abstract 242.
124. Thomas, C.K. & Ross, B.H. 1997. Distinct patterns of motor unit behavior during muscle spasms in spinal cord injured subjects. J Neurophysiol 77, 2847-2850.
125. Thomas, C.K. & Zijdewind, I. 2006. Fatigue of muscles weakened by death of motoneurons. Muscle Nerve 33, 21-41.
126. Thomas, C.K., Ross, B.H. & Stein, R.B. 1986. Motor-unit recruitment in human first dorsal interosseous muscle for static contractions in three different directions. J Neurophysiol 55, 1017-1029.
127. Thomas, C.K., Ross, B.H. & Calancie, B. 1987. Human motor-unit recruitment during isometric contractions and repeated dynamic movements. J Neurophysiol 57, 311-324.
128. Thomas, C.K., Johansson, R.S., Westling, G. & Bigland-Ritchie, B. 1990. Twitch properties of human thenar motor units measured in response to intraneural motor-axon stimulation. J Neurophysiol 64, 1339-1346.
129. Thomas, C.K., Bigland-Ritchie, B. & Johansson, R.S. 1991a. Force-frequency relationships of human thenar motor units. J Neurophysiol 65, 1509-1516.
130. Thomas, C.K., Johansson, R.S. & Bigland-Ritchie, B. 1991b. Attempts to physiologically classify human thenar motor units. J Neurophysiol 65, 1501-1508.
131. Thomas, C.K., Broton, J.G. & Calancie, B. 1997a. Motor unit forces and recruitment patterns after cervical spinal cord injury. Muscle Nerve 20, 212-220.
132. Thomas, C.K., Zaidner, E.Y., Calancie, B., Broton, J.G. & Bigland-Ritchie, B.R. 1997b. Muscle weakness, paralysis and atrophy after human cervical spinal cord injury. Exp Neurol 148, 414-423.
133. Thomas, C.K., Tucker, M.E. & Bigland-Ritchie, B. 1998. Voluntary muscle weakness and co-activation after chronic cervical spinal cord injury. J Neurotrauma 15, 149-161.
134. Thomas, C.K., Butler, J.E. & Zijdewind, I. 2002a. Patterns of pathological firing in human motor units. Adv Exp Med Biol 508, 237-244.
135. Thomas, C.K., Nelson, G., Than, L. & Zijdewind, I. 2002b. Motor unit activation order during electrically evoked contractions of paralyzed or partially paralyzed muscles. Muscle Nerve 25, 797-804.
136. Thomas, C.K., Griffin, L., Godfrey, S., Ribot-Ciscar, E. & Butler, J.E. 2003. Fatigue of paralyzed and control thenar muscles induced by variable or constant frequency stimulation. J Neurophysiol 89, 2055-2064.
137. Thomas, C.K., Häger-Ross, C.K. & Klein, C.S. 2010. Effects of baclofen on motor units paralysed by chronic cervical spinal cord injury. Brain 133, 117-125.
138. Thomas, C.K., Häger, C.K. & Klein, C.S. 2011. F-waves in motor units paralyzed by human spinal cord injury. Society for Neuroscience, Abstract. 278.04.
139. Thompson, A.K., Pomerantz, F.R. & Wolpaw, J.R. 2013. Operant conditioning of a spinal reflex can improve locomotion after spinal cord injury in humans. J Neurosci 33, 2365-2375.
140. Triolo, R.J., Bailey, S.N., Miller, M.E., Rohde, L.M., Anderson, J.S., Davis, J.A. Jr, Abbas, J.J., DiPonio, L.A., Forrest, G.P., Gater, D.R. Jr & Yang, L.J. 2012. Longitudinal performance of a surgically implanted neuroprosthesis for lower-extremity exercise, standing, and transfers after spinal cord injury. Arch Phys Med Rehabil 93, 896-904.
141. Van Cutsem, M., Feiereisen, P., Duchateau, J. & Hainaut, K. 1997. Mechanical properties and behaviour of motor units in the tibialis anterior during voluntary contractions. Can J Appl Physiol 22, 585-597.
142. Wiegner, A.W., Wierzbicka, M.M., Davies, L. & Young, R.R. 1993. Discharge properties of single motor units in patients with spinal cord injuries. Muscle Nerve 16, 661-671.
143. Wise, A.K., Morgan, D.L., Gregory, J.E. & Proske, U. 2001. Fatigue in mammalian skeletal muscle stimulated under computer control. J Appl Physiol 90, 189-197.
144. Yang, J.F., Stein, R.B., Jhamandas, J. & Gordon, T. 1990. Motor unit numbers and contractile properties after spinal cord injury. Ann Neurol 28, 496-502.
145. Zaaimi, B., Edgley, S.A., Soteropoulos, D.S. & Baker, S.N. 2012. Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey. Brain 135, 2277-2289.
146. Zijdewind, I. & Thomas, C.K. 2001. Spontaneous motor unit behavior in human thenar muscles after spinal cord injury. Muscle Nerve 24, 952-962.
147. Zijdewind, I. & Thomas, C.K. 2003. Motor unit firing during and after voluntary contractions of human thenar muscles weakened by spinal cord injury. J Neurophysiol 89, 2065-2071.
148. Zijdewind, I. & Thomas, C.K. 2012. Firing patterns of spontaneously active motor units in spinal cord-injured subjects. J Physiol (Lond) 590, 1683-1697.
149. Zijdewind, I., Kernell, D. & Kukulka, C.G. 1995. Spatial differences in fatigue-associated electromyographic behaviour of the human first dorsal interosseus muscle. J Physiol (Lond) 483, 499-509.
150. Zijdewind, I., Gant, K., Bakels, R. & Thomas, C.K. 2012. Do additional inputs change maximal voluntary motor unit firing rates after spinal cord injury? Neurorehabil Neural Repair 26, 58-67.