Origins of spontaneous firing of motor units in the spastic-paretic biceps brachii muscle of stroke survivors

Journal of Neurophysiology

Volumn 104, Issue 6, 2010, Pages 3168-3179

  Mottram, C J ^a   Wallace, C L ^a   Chikando, C N ^a   Rymer, W Z ^a  

^a REHABILITATION INSTITUTE OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; BICEPS BRACHII MUSCLE; CLINICAL ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; FEMALE; HEMIPARESIS; HUMAN; MALE; MOTONEURON; MOTOR UNIT; MUSCLE SPASM; NERVE CELL STIMULATION; PARESIS; PRIORITY JOURNAL; STROKE;

ACTION POTENTIALS; AGED; ARM; FEMALE; HUMANS; INTERNEURONS; MALE; MATCHED-PAIR ANALYSIS; MIDDLE AGED; MODELS, NEUROLOGICAL; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE SPASTICITY; MUSCLE, SKELETAL; PARESIS; STROKE;

EID: 78650907867     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00463.2010     Document Type: Article

References (80)

1. Andrews C, Knowles L, Hancock J. Control of the tonic vibration reflex by the brain stem reticular formation in the cat. J Neurol Sci 18: 217-226, 1973b.
2. Andrews C, Knowles L, Lance JW. Corticoreticulospinal control of the tonic vibration reflex in the cat. J Neurol Sci 18: 207-216, 1973a.
3. Aymard C, Katz R, Lafitte C, Lo E, Penicaud A, Pradat-Diehl P, Raoul S. Presynaptic inhibition and homosynaptic depression: A comparison between lower and upper limbs in normal human subjects and patients with hemiplegia. Brain 123: 1688-1702, 2000.
4. Barzi Y, Zehr EP. Rhythmic arm cycling suppresses hyperactive soleus H-reflex amplitude after stroke. Clin Neurophysiol 119: 1443-1452, 2008.
5. Bennett DJ, Hultborn H, Fedirchuk B, Gorassini M. Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. J Neurophysiol 80: 2023-2037, 1998. (Pubitemid 28489130)
6. Bennett DJ, Li Y, Harvey PJ, Gorassini M. Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. J Neurophysiol 86: 1972-1982, 2001a.
7. Bennett DJ, Li Y, Siu M. Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. J Neurophysiol 86: 1955-1971, 2001b. (Pubitemid 32953241)
8. Buchanan JT, Kasicki S. Segmental distribution of common synaptic inputs to spinal motoneurons during fictive swimming in the lamprey. J Neurophysiol 82: 1156-1163, 1999.
9. Burke D, Andrews CJ, Gillies JD. Reflex response to sinusoidal stretch in spastic man. Brain 94: 455-470, 1971a.
10. Burke D, Ashby P. Are spinal "presynaptic" inhibitory mechanisms suppressed in spasticity? J Neurol Sci 15: 321-326, 1972.
11. Burke D, Gillies JD, Lance JW. Hamstrings stretch reflex in human spasticity. J Neurol Neurosurg Psychiatry 34: 231-235, 1971b.
12. Burke D, Knowles L, Andrews C, Ashby P. Spasticity, decerebrate rigidity and the clasp-knife phenomenon: An experimental study in the cat. Brain 95: 31-48, 1972.
13. Chardon MK, Suresh NL, Rymer WZ. Reflex threshold estimation in spastic muscles: A new method. Program No. 76.4/NN12. 2008 Abstract Viewer/ Itinerary Planner. Washington, DC: Society for Neuroscience, 2008. Online.
14. Christou EA, Rudrof T, Enoka JA, Meyer F, Enoka RM. Discharge rate during low-force isometric contractions influences motor unit coherence below 15 Hz but not motor unit synchronization. Exp Brain Res 178: 285-295, 2007.
15. Chung SG, van Rey E, Bai Z, Rymer WZ, Roth EJ, Zhang LQ. Separate quantification of reflex and nonreflex components of spastic hypertonia in chronic hemiparesis. Arch Phys Med Rehabil 89: 700-710, 2008.
16. Conway BA, Halliday DM, Farmer SF, Shahani U, Maas P, Weir AI, Rosenberg JR. Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. J Physiol 489: 917-924, 1995.
17. Crone C, Johnsen LL, Biering-Sorensen F, Nielsen JB. Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain 126: 495-507, 2003.
18. Datta AK, Stephens JA. Synchronization of motor unit activity during voluntary contraction in man. J Physiol 422: 397-419, 1990.
19. De Luca CJ, Erim Z. Common drive of motor units in regulation of muscle force. Trends Neurosci 17: 299-305, 1994.
20. Eken T, Hultborn H, Kiehn O. Possible functions of transmitter-controlled plateau potentials in alpha motoneurones. Prog Brain Res 80: 257-267, 1989.
21. Farmer SF, Bremner FD, Halliday DM, Rosenberg JR, Stephens JA. The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. J Physiol 470: 127-155, 1993a.
22. Farmer SF, Halliday DM, Conway BA, Stephens JA, Rosenberg JR. A review of recent applications of cross-correlation methodologies to human motor unit recording. J Neurosci Methods 74: 175-187, 1997.
23. Farmer SF, Swash M, Ingram DA, Stephens JA. Changes in motor unit synchronization following central nervous lesions in man. J Physiol 463: 83-105, 1993b.
24. Gorassini M, Yang JF, Siu M, Bennett DJ. Intrinsic activation of human motoneurons: Reduction of motor unit recruitment thresholds by repeated contractions. J Neurophysiol 87: 1859-1866, 2002.
25. Gorassini MA, Knash ME, Harvey PJ, Bennett DJ, Yang JF. Role of motoneurons in the generation of muscle spasms after spinal cord injury. Brain 127: 2247-2258, 2004.
26. Gregson JM, Leathley MJ, Moore AP, Smith TL, Sharma AK, Watkins CL. Reliability of measurements of muscle tone and muscle power in stroke patients. Age Ageing 29: 223-228, 2000.
27. Halliday DM, Conway BA, Farmer SF, Rosenberg JR. Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans. Neurosci Lett 241: 1-4, 1998.
28. Halliday DM, Rosenberg JR. Time and frequency domain analysis of spike train and time series data. In: Modern Techniques in Neuroscience Research, edited by Windhorst U, Johansson H. New York: Springer-Verlag, 1999, p. 503-543.
29. Harris-Warrick RM, Cohen AH. Serotonin modulates the central pattern generator for locomotion in the isolated lamprey spinal cord. J Exp Biol 116: 27-46, 1985.
30. Harvey PJ, Li X, Li Y, Bennett DJ. 5-ht2 Receptor activation facilitates a persistent sodium current and repetitive firing in spinal motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 96: 1158-1170, 2006.
31. Heckman CJ, Lee RH, Brownstone RM. Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci 26: 688-695, 2003.
32. Holstege JC, Kuypers HGJM. Brainstem projections to spinal motoneurones: An update. Neuroscience 23: 809-821, 1987.
33. Hornby TG, Heckman CJ, Harvey RL, Rymer WZ. Changes in voluntary torque and electromyographic activity following oral baclofen. Muscle Nerve 30: 784-795, 2004.
34. Hounsgaard J, Kiehn O. Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J Physiol 414: 265-282, 1989.
35. Hultborn H. Changes in neuronal properties and spinal reflexes during development of spasticity following spinal cord lesions and stroke: Studies in animal models and patients. J Rehabil Med 35, Suppl. 41: 46-55, 2003.
36. Katz RT, Rymer WZ. Spastic hypertonia: Mechanisms and measurement. Arch Phys Med Rehabil 70: 144-155, 1989.
37. Kilner JM, Alonso-Alonso M, Fisher R, Lemon RN. Modulation of synchrony between single motor units during precision grip tasks in humans. J Physiol 541: 937-948, 2002.
38. Kirkwood PA, Sears TA. The synaptic connexions to intercostal motoneurons as revealed by their average common excitation potential. J Physiol 275: 103-134, 1978.
39. Kline TL, Schmit BD, Kamper DG. Exaggerated interlimb neural coupling following stroke. Brain 130: 159-169, 2007.
40. Krawitz S, Fedirchuk B, Dai Y, Jordan LM, McCrea DA. State-dependent hyperpolarization of voltage threshold enhances motoneurone excitability during fictive locomotion in the cat. J Physiol 532: 271-281, 2001.
41. Lamy JC, Wargon I, Mazevet D, Ghanim Z, Pradat-Diehl P, Katz R. Impaired efficacy of spinal presynaptic mechanisms in spastic stroke patients. Brain 132: 734-748, 2009.
42. Lance JW. The control of muscle tone, reflexes, and movement: Robert Wartenberg Lecture. Neurology 30: 1303-1313, 1980.
43. Lance JW. Disordered muscle tone and movement. Clin Exp Neurol 18: 27-35, 1981.
44. Lee RH, Heckman CJ. Influence of voltage-sensitive dendritic conductances on bistable firing and effective synaptic current in cat spinal motoneurons in vivo. J Neurophysiol 76: 2107-2110, 1996.
45. Lee RH, Heckman CJ. Bistability in spinal motoneurons in vivo: Systematic variations in rhythmic firing patterns. J Neurophysiol 80: 572-582, 1998a.
46. Lee RH, Heckman CJ. Bistability in spinal motoneurons in vivo: Systematic variations in persistent inward currents. J Neurophysiol 80: 583-593, 1998b.
47. Lee RH, Heckman CJ. Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J Neurosci 20: 6734-6740, 2000.
48. Lee RH, Kuo JJ, Jiang MC, Heckman CJ. Influence of active dendritic currents on input- output processing in spinal motoneurons in vivo. J Neurophysiol 89: 27-39, 2003.
49. Lewek MD, Hornby TG, Dhaher YY, Schmit BD. Prolonged quadriceps activity following imposed hip extension: A neurophysiological mechanism for stiff-knee gait? J Neurophysiol 98: 3153-3162, 2007.
50. Li Y, Bennett DJ. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90: 857-869, 2003.
51. Li Y, Gorassini MA, Bennett DJ. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 91: 767-783, 2004. (Pubitemid 38168850)
52. Litvan I, Mangone CA, Werden W, Bueri JA, Estol CJ, Garcea DO, Rey RC, Sica RE, Hallett M, Bartko JJ. Reliability of the NINDS myotatic reflex scale. Neurology 47: 969-972, 1996.
53. Lukacs M. Electrophysiological signs of changes in motor units after ischaemic stroke. Clin Neurophysiol 116: 1566-1570, 2005.
54. Mazzaro N, Nielsen JF, Grey MJ, Sinkjaer T. Decreased contribution from afferent feedback to the soleus muscle during walking in patients with spastic stroke. J Stroke Cerebrovasc Dis 16: 135-144, 2007.
55. McPherson JG, Ellis MD, Heckman C, Dewald JP. Evidence for increased activation of persistent inward currents in individuals with chronic hemiparetic stroke. J Neurophysiol 100: 3236-3243, 2008.
56. Merletti R, Rainoldi A, Farina D. Surface electromyography for noninvasive characterization of muscle. Exerc Sport Sci Rev 29: 20-25, 2001.
57. Mirbagheri MM, Alibiglou L, Thajchayapong M, Rymer WZ. Muscle and reflex changes with varying joint angle in hemiparetic stroke (Abstract). J Neuroeng Rehabil 5: 6, 2008.
58. Moritz CT, Christou EA, Meyer FG, Enoka RM. Coherence at 16-32 Hz can be caused by short-term synchrony of motor units. J Neurophysiol 94: 105-118, 2005.
59. Mottram CJ, Suresh NL, Heckman CJ, Gorassini MA, Rymer WZ. Origins of abnormal excitability in biceps brachii motoneurons of spastic- paretic stroke survivors. J Neurophysiol 102: 2026-2038, 2009a.
60. Mottram CJ, Wallace CL, Chikando CN, Meyer FG, Rymer WZ. Spontaneously firing motor unit pairs in the spastic biceps brachii of stroke survivors are co-modulated. Program No. 659.17/CC9. 2009 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2009b. Online.
61. Mottram CJ, Wallace CL, Chikando CN, Rymer WZ. Mechanisms contributing to spontaneous firing of motor units in the spastic biceps brachii of stroke survivors. Program No. 726.10. 2007 Abstract Viewer/Itinerary Planner. San Diego, CA: Society for Neuroscience, 2007. Online.
62. Myers LJ, Erim Z, Lowery MM. Time and frequency domain methods for quantifying common modulation of motor unit firing patterns (Abstract). J Neuroeng Rehabil 1: 2, 2004.
63. Nielsen J, Hultborn H. Regulated properties of motoneurons and primary afferents: New aspects on possible spinal mechanisms underlying spasticity. In: Spasticity: Mechanisms and Management, edited by Thilmann AF. Berlin: Springer-Verlag, 1993, p. 177-191.
64. Nordstrom MA, Fuglevand AJ, Enoka RM. Estimating the strength of common input to human motoneurons from the cross-correlogram. J Physiol 453: 547-574,1992.
65. Person RS, Kudina LP. Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle. Electroencephalogr Clin Neurophysiol 32: 471-483, 1972.
66. Pettersen V, Bjorkoy K, Torp H, Westgaard RH. Neck and shoulder muscle activity and thorax movement in singing and speaking tasks with variation in vocal loudness and pitch. J Voice 19: 623-634, 2005.
67. Pettersen V, Westgaard RH. The activity patterns of neck muscles in professional classical singing. J Voice 19: 238-251, 2005.
68. Pierucci M, Di Matteo V, Benigno A, Crescimanno G, Esposito E, Di Giovanni G. The unilateral nigral lesion induces dramatic bilateral modification on rat brain monoamine neurochemistry. Ann NY Acad Sci 1155: 316-323, 2009.
69. Powers RK, Binder MD. Input- output functions of mammalian motoneurons. Rev Physiol Biochem Pharmacol 143: 137-263, 2001.
70. Powers RK, Marder-Meyer J, Rymer WZ. Quantitative relations between hypertonia and stretch reflex threshold in spastic hemiparesis. Ann Neurol 23: 115-124, 1988.
71. Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, Halliday DM. The Fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol 53: 1-31, 1989.
72. Schwindt PC, Crill WE. Factors influencing motoneuron rhythmic firing: Results from a voltage-clamp study. J Neurophysiol 48: 875-890, 1982.
73. Sears TA, Stagg D. Short-term synchronization of intercostal motoneurone activity. J Physiol 263: 357-381, 1976.
74. Seki K, Perlmutter SI, Fetz EE. Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat Neurosci 6: 1309-1316, 2003.
75. Semmler JG, Kornatz KW, Enoka RM. Motor-unit coherence during isometric contractions is greater in a hand muscle of older adults. J Neurophysiol 90: 1346-1349, 2003.
76. Semmler JG, Sale MV, Meyer FG, Nordstrom MA. Motor unit coherence and its relation with synchrony are influenced by training. J Neurophysiol 92: 3320-3331, 2004.
77. Suresh NL, Ellis MD, Moore J, Heckman H, Rymer WZ. Excitatory synaptic potentials in spastic human motoneurons have a short rise-time. Muscle Nerve 32: 99-103, 2005.
78. Svirskis G, Hounsgaard J. Transmitter regulation of plateau properties in turtle motoneurons. J Neurophysiol 79: 45-50, 1998.
79. Westgaard RH, Bonato P, Westad C. Respiratory and stress-induced activation of low-threshold motor units in the human trapezius muscle. Exp Brain Res 175: 689-701, 2006.
80. Zijdewind I, Thomas CK. Spontaneous motor unit behavior in human thenar muscles after spinal cord injury. Muscle Nerve 24: 952-962, 2001.