Influence of fatigue on hand muscle coordination and EMG-EMG coherence during three-digit grasping

Journal of Neurophysiology

Volumn 104, Issue 6, 2010, Pages 3576-3587

  Santos, Alessander Danna Dos ^a   Poston, Brach ^a   Jesunathadas, Mark ^a   Bobich, Lisa R ^a   Hamm, Thomas M ^b   Santello, Marco ^a  

^a Arizona State University   (United States)

^b BARROW NEUROLOGICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; ELECTROMYOGRAPHY; FEMALE; HAND MUSCLE; HUMAN; INDEX FINGER; MALE; MOTONEURON NUCLEUS; MUSCLE CONTRACTION; MUSCLE FATIGUE; PRIORITY JOURNAL; THUMB;

ADULT; ELECTROMYOGRAPHY; FEMALE; FINGERS; HAND; HAND STRENGTH; HUMANS; ISOMETRIC CONTRACTION; MALE; MUSCLE FATIGUE; MUSCLE, SKELETAL; YOUNG ADULT;

EID: 78650858447     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00583.2010     Document Type: Article

References (78)

1. Amjad AM, Halliday DM, Rosenberg JR, Conway BA. An extended difference of coherence test for comparing and combining several independent coherence estimates: Theory and application to the study of motor units and physiological tremor. J Neurosci Methods 73: 69-79, 1997.
2. Baker SN. Quantification of the relative efficacies of asynchronous and oscillating inputs to a motoneurone pool using a computer model. J Physiol 504: 116P, 1997.
3. Baker SN, Kilner JM, Pinches EM, Lemon RN. The role of synchrony and oscillations in the motor output. Exp Brain Res 128: 109-117, 1999.
4. Bigland-Ritchie B, Johansson R, Lippold OC, Smith S, Woods JJ. Changes in motoneuron firing rates during sustained maximal voluntary contractions. J Physiol 340: 335-346, 1983a.
5. Bigland-Ritchie BR, Dawson NJ, Johansson RS, Lippold OC. Reflex origin for the slowing of motoneuron firing rates in fatigue of human voluntary contractions. J Physiol 379: 451-459, 1986.
6. Bigland-Ritchie B, Johansson R, Lippold OC, Woods JJ. Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J Neurophysiol 50: 313-324, 1983b.
7. Bigland-Ritchie B, Rice CL, Garland SJ, Walsh ML. Task-dependent factors in fatigue of human voluntary contractions. Adv Exp Med Biol 384: 361-380, 1995.
8. Bigland-Ritchie B, Woods JJ. Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 7: 691-699, 1984.
9. Bongiovanni LG, Hagbarth KE. Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man. J Physiol 423: 1-14, 1990.
10. Bongiovanni LG, Hagbarth KE, Stjernberg L. Prolonged muscle vibration reducing motor output in maximal voluntary contractions in man. J Physiol 423: 15-26, 1990.
11. Brown P. Cortical drives to human muscle: The Piper and related rhythms. Prog Neurobiol 60: 97-108, 2000.
12. Carpentier A, Duchateau J, Hainaut K. Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus. J Physiol 534: 903-912, 2001.
13. Christova P, Kossev A. Human motor unit recruitment and derecruitment during long lasting intermittent contractions. J Electromyogr Kinesiol 11: 189-196, 2001.
14. Cresswell AG, Loscher WN. Significance of peripheral afferent input to the alpha-motoneuron pool for enhancement of tremor during an isometric fatiguing contraction. Eur J Appl Physiol 82: 129-136, 2000.
15. Danion F, Latash ML, Li ZM, Zatsiorsky VM. The effect of fatigue on multifinger co-ordination force production tasks in humans. J Physiol 523: 523-532, 2000.
16. Danion F, Latash ML, Li ZM, Zatsiorsky VM. The effect of fatiguing exercise by the index finger on single- and multi-finger force production. Exp Brain Res 138: 322-329, 2001.
17. De Luca CJ, LeFever RS, McCue MP, Xenakis AP. Control scheme governing concurrently active human motor units during voluntary contractions. J Physiol 329: 129-142, 1982.
18. Ebenbichler GR, Kollmitzer J, Erim Z, Loscher WN, Kerschan K, Posch M, Nowotny T, Kranzl A, Wober C, Bochdansky T. Load-dependence of fatigue related changes in tremor around 10 Hz. Clin Neurophysiol 111: 106-111, 2000.
19. Enoka RM, Duchateau J. Muscle fatigue: What, why and how it influences muscle function. J Physiol 586: 11-23, 2008.
20. Enoka RM, Stuart DG. Neurobiology of muscle fatigue. J Appl Physiol 72: 1631-1648, 1992.
21. Fallentin N, Jorgensen K, Simonsen EB. Motor unit recruitment during prolonged isometric contractions. Eur J Appl Physiol Occup Physiol 67: 335-341, 1993.
22. Farmer SF. Rhythmicity, synchronization and binding in human and primate motor systems. J Physiol 509: 3-14, 1998.
23. 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, 1993.
24. Fisher RJ, Galea MP, Brown P, Lemon RN. Digital nerve anaesthesia decreases EMG-EMG coherence in a human precision grip task. Exp Brain Res 145: 207-214, 2002.
25. Fuglevand AJ, Zackowski KM, Huey KA, Enoka RM. Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol 460: 549-572, 1993.
26. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81: 1725-1789, 2001.
27. Gandevia SC, Allen GM, Butler JE, Taylor JL. Supraspinal factors in human muscle fatigue: Evidence for suboptimal output from the motor cortex. J Physiol 490: 529-536, 1996.
28. Grosse P, Cassidy MJ, Brown P. EEG-EMG, MEG-EMG and EMG-EMG frequency analysis: Physiological principles and clinical applications. Clin Neurophysiol 113: 1523-1531, 2002.
29. Halliday DM, Rosenberg JR, Rigas A, Conway BA. A periodogram-based test for weak stationarity and consistency between sections in time series. J Neurosci Methods 180: 138-146, 2009.
30. Hunter SK, Enoka RM. Changes in muscle activation can prolong the endurance time of a submaximal isometric contraction in humans. J Appl Physiol 94: 108-118, 2003.
31. Hunter SK, Ryan DL, Ortega JD, Enoka RM. Task differences with the same load torque alter the endurance time of submaximal fatiguing contractions in humans. J Neurophysiol 88: 3087-3096, 2002.
32. Kato M, Murakami S, Takahashi K, Hirayama H. Motor unit activities during maintained voluntary muscle contraction at constant levels in man. Neurosci Lett 25: 149-154, 1981.
33. Kattla S, Lowery MM. Fatigue related changes in electromyographic coherence between synergistic hand muscles. Exp Brain Res 2009.
34. Kidgell DJ, Sale MV, Semmler JG. Motor unit synchronization measured by cross-correlation is not influenced by short-term strength training of a hand muscle. Exp Brain Res 175: 745-753, 2006.
35. 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.
36. Kilner JM, Baker SN, Salenius S, Jousmaki V, Hari R, Lemon RN. Task-dependent modulation of 15-30 Hz coherence between rectified EMGs from human hand and forearm muscles. J Physiol 516: 559-570, 1999.
37. Kilner JM, Fisher RJ, Lemon RN. Coupling of oscillatory activity between muscles is strikingly reduced in a deafferented subject compared with normal controls. J Neurophysiol 92: 790-796, 2004.
38. Klass M, Levenez M, Enoka RM, Duchateau J. Spinal mechanisms contribute to differences in the time to failure of submaximal fatiguing contractions performed with different loads. J Neurophysiol 99: 1096-1104, 2008.
39. Kouzaki M, Shinohara M. The frequency of alternate muscle activity is associated with the attenuation in muscle fatigue. J Appl Physiol 101: 715-720, 2006.
40. Kouzaki M, Shinohara M, Masani K, Fukunaga T. Force fluctuations are modulated by alternate muscle activity of knee extensor synergists during low-level sustained contraction. J Appl Physiol 97: 2121-2131, 2004.
41. Kouzaki M, Shinohara M, Masani K, Kanehisa H, Fukunaga T. Alternate muscle activity observed between knee extensor synergists during low-level sustained contractions. J Appl Physiol 93: 675-684, 2002.
42. Kouzaki M, Shinohara M, Masani K, Tachi M, Kanehisa H, Fukunaga T. Local blood circulation among knee extensor synergists in relation to alternate muscle activity during low-level sustained contraction. J Appl Physiol 95: 49-56, 2003.
43. Levenez M, Garland SJ, Klass M, Duchateau J. Cortical and spinal modulation of antagonist coactivation during a submaximal fatiguing contraction in humans. J Neurophysiol 99: 554-563, 2008.
44. Llinas R, Jahnsen H. Electrophysiology of mammalian thalamic neurons in vitro. Nature 297: 406-408, 1982.
45. Llinas R, Yarom Y. Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurons in vitro. J Physiol 315: 569-584, 1981.
46. Maris E, Schoffelen JM, Fries P. Nonparametric statistical testing of coherence differences. J Neurosci Methods 163: 161-175, 2007.
47. Martin PG, Smith JL, Butler JE, Gandevia SC, Taylor JL. Fatiguesensitive afferents inhibit extensor but not flexor motoneurons in humans. J Neurosci 26: 4796-4802, 2006.
48. McAuley JH, Marsden CD. Physiological and pathological tremors and rhythmic central motor control. Brain 123: 1545-1567, 2000.
49. McAuley JH, Rothwell JC, Marsden CD. Frequency peaks of tremor, muscle vibration and electromyographic activity at 10 Hz, 20 Hz and 40 Hz during human finger muscle contraction may reflect rhythmicities of central neural firing. Exp Brain Res 114: 525-541, 1997.
50. McIsaac TL, Fuglevand AJ. Common synaptic input across motor nuclei supplying intrinsic muscles involved in the precision grip. Exp Brain Res 188: 159-164, 2008.
51. Mima T, Simpkins N, Oluwatimilehin T, Hallett M. Force level modulates human cortical oscillatory activities. Neurosci Lett 275: 77-80, 1999.
52. Moritz CT, Barry BK, Pascoe MA, Enoka RM. Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. J Neurophysiol 93: 2449-2459, 2005.
53. Mottram CJ, Christou EA, Meyer FG, Enoka RM. Frequency modulation of motor unit discharge has task-dependent effects on fluctuations in motor output. J Neurophysiol 94: 2878-2887, 2005a.
54. Mottram CJ, Jakobi JM, Semmler JG, Enoka RM. Motor-unit activity differs with load type during a fatiguing contraction. J Neurophysiol 93: 1381-1392, 2005b.
55. Mottram CJ, Maluf KS, Stephenson JL, Anderson MK, Enoka RM. Prolonged vibration of the biceps brachii tendon reduces time to failure when maintaining arm position with a submaximal load. J Neurophysiol 95: 1185-1193, 2006.
56. Murthy VN, Fetz EE. Effects of input synchrony on the firing rate of a 3-conductance cortical neuron model. Neural Comput 6: 1111-1126, 1994.
57. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: A primer with examples. Hum Brain Mapp 15: 1-25, 2002.
58. Palmer E, Ashby P. Corticospinal projections to upper limb motoneurons in humans. J Physiol 448: 397-412, 1992.
59. Person RS. Rhythmic activity of a group of human motoneurons during voluntary contraction of a muscle. Electroencephalogr Clin Neurophysiol 36: 585-595, 1974.
60. Poston B, Danna-Dos Santos A, Bobich LR, Santello M. The influence of fatigue on hand muscle coordination and EMG-EMG coherence during three-digit grasping. Soc Neurosci Abstr 862.21, 2009.
61. Poston B, Danna-Dos Santos A, Jesunathadas M, Hamm TM, Santello M. Force-independent distribution of correlated neural inputs to hand muscles during three-digit grasping. J Neurophysiol 104: 1141-1154, 2010.
62. Riddle CN, Baker SN. Manipulation of peripheral neural feedback loops alters human corticomuscular coherence. J Physiol 566: 625-639, 2005.
63. 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.
64. Rudroff T, Christou EA, Poston B, Bojsen-Moller J, Enoka RM. Time to failure of a sustained contraction is predicted by target torque and initial electromyographic bursts in elbow flexor muscles. Muscle Nerve 35: 657-666, 2007.
65. Rudroff T, Poston B, Shin IS, Bojsen-Moller J, Enoka RM. Net excitation of the motor unit pool varies with load type during fatiguing contractions. Muscle Nerve 31: 78-87, 2004.
66. Sale DG. Influence of exercise and training on motor unit activation. Exerc Sport Sci Rev 15: 95-151, 1987.
67. Schoffelen JM, Oostenveld R, Fries P. Neuronal coherence as a mechanism of effective corticospinal interaction. Science 308: 111-113, 2005.
68. 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.
69. Shinohara M, Yoshitake Y, Kouzaki M. Alterations in synergistic muscle activation impact fluctuations in net force. Med Sci Sports Exerc 41: 191-197, 2009.
70. Singh T, Varadhan SK, Zatsiorsky VM, Latash ML. Fatigue and motor redundancy: Adaptive increase in finger force variance in multi-finger tasks. J Neurophysiol 103: 2990-3000.
71. Sjogaard G, Kiens B, Jorgensen K, Saltin B. Intramuscular pressure, EMG and blood flow during low-level prolonged static contraction in man. Acta Physiol Scand 128: 475-484, 1986.
72. Taylor JL, Butler JE, Gandevia SC. Changes in muscle afferents, motoneurons and motor drive during muscle fatigue. Eur J Appl Physiol 83: 106-115, 2000.
73. Taylor JL, Gandevia SC. A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104: 542-550, 2008.
74. Valero-Cuevas FJ. Predictive modulation of muscle coordination pattern magnitude scales fingertip force magnitude over the voluntary range. J Neurophysiol 83: 1469-1479, 2000.
75. Valero-Cuevas FJ, Zajac FE, Burgar CG. Large index-fingertip forces are produced by subject-independent patterns of muscle excitation. J Biomech 31: 693-703, 1998.
76. Westgaard RH, de Luca CJ. Motor unit substitution in long-duration contractions of the human trapezius muscle. J Neurophysiol 82: 501-504, 1999.
77. Winges SA, Kornatz KW, Santello M. Common input to motor units of intrinsic and extrinsic hand muscles during two-digit object hold. J Neurophysiol 99: 1119-1126, 2008.
78. Winges SA, Santello M. Common input to motor units of digit flexors during multi-digit grasping. J Neurophysiol 92: 3210-3220, 2004.