The extraction of neural strategies from the surface EMG: An update

Journal of Applied Physiology

Volumn 117, Issue 11, 2014, Pages 1215-1230

  Farina, Dario ^a   Merletti, Roberto ^b   Enoka, Roger M ^c  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b POLITECNICO DI TORINO   (Italy)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Amplitude cancellation; Coherence; Decomposition; Motor neuron; Motor unit; Neural drive to muscle; Rectification; Spectral analysis; Surface EMG

Indexed keywords

ELECTROMYOGRAPHY; HUMAN; MOTONEURON; NEUROMUSCULAR JUNCTION; PHYSIOLOGY;

ELECTROMYOGRAPHY; HUMANS; MOTOR NEURONS; NEUROMUSCULAR JUNCTION;

EID: 84904310636     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00162.2014     Document Type: Article

References (106)

1. Andreassen S, Arendt-Nielsen L. Muscle fibre conduction velocity in motor units of the human anterior tibial muscle: A new size principle parameter. J Physiol 391: 561-571, 1987.
2. Baker SN, Olivier E, Lemon RN. Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J Physiol 501: 225-241, 1997.
3. Bankman I, Johnson K, Schneider K. Optimal detection, classification, and superposition resolution in neural waveform recordings. IEEE Trans Biomed Eng 8: 836-841, 1993.
4. Blok JH, van Dijk JP, Drost G, Zwarts MJ, Stegeman DF. A high-density multichannel surface electromyography system for the characterization of single motor units. Rev Sci Instrum 73: 1887-1897, 2002.
5. Blok JH, Stegeman DF, van Oosterom A. Three-layer volume conductor model and software package for applications in surface electromyography. Ann Biomed Eng 30: 566-577, 2002.
6. Boonstra TW, Daffertshofer A, van As E, van der Vlugt S, Beek PJ. Bilateral motor unit synchronization is functionally organized. Exp Brain Res 178: 79-88, 2007.
7. Boonstra TW, Breakspear M. Neural mechanisms of intermuscular coherence: Implications for the rectification of surface electromyography. J Neurophysiol 107: 796-807, 2012.
8. Clancy EA, Hogan N. Single site electromyograph amplitude estimation. IEEE Trans Biomed Eng 41: 159-167, 1994.
9. 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.
10. Danna-Dos Santos A., Poston B., Jesunathadas M., Bobich LR, Hamm TM, Santello M. Influence of fatigue on hand muscle coordination and EMG-EMG coherence during three-digit grasping. J Neurophysiol 104: 3576-3587, 2010.
11. Day SJ, Hulliger M. Experimental simulation of cat electromyogram: Evidence for algebraic summation of motor-unit action-potential trains. J Neurophysiol 86: 2144-2158, 2001.
12. De Luca CJ, Merletti R. Surface myoelectric signal cross-Talk among muscles of the leg. Electroencephalogr Clin Neurophysiol 69: 568-575, 1988.
13. De Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 13: 135-163, 1997.
14. De Luca CJ, Adam A, Wotiz R, Gilmore LD, Nawab SH. Decomposition of surface EMG signals. J Neurophysiol 96: 1646-1657, 2006.
15. De Luca CJ, Erim Z. Common drive of motor units in regulation of muscle force. Trends Neurosci 17: 299-305, 1994.
16. De Luca CJ, Hostage EC. Relationship between firing rate and recruitment threshold of motoneurons in voluntary isometric contractions. J Neurophysiol 104: 1034-1046, 2010.
17. De Luca CJ, Nawab SH. Reply to Farina and Enoka: The reconstructand-Test approach is the most appropriate validation for surface EMG signal decomposition to date. J Neurophysiol 105: 983-984, 2011.
18. Deschenes MR, Giles JA, McCoy RW, Volek JS, Gomez AL, Kraemer WJ. Neural factors account for strength decrements observed after short-Term muscle unloading. Am J Physiol Regul Integr Comp Physiol 282: R578-R583, 2002.
19. Dideriksen JL, Farina D, Baekgaard M, Enoka RM. An integrative model of motor unit activity during sustained submaximal contractions. J Appl Physiol 108: 1550-1562, 2010.
20. Dideriksen JL, Negro F, Enoka RM, Farina D. Motor unit recruitment strategies and muscle properties determine the influence of synaptic noise on force steadiness. J Neurophysiol 107: 3357-3369, 2012.
21. Dimitrov GV, Arabadzhiev TI, Hogrel JY, Dimitrova NA. Simulation analysis of interference EMG during fatiguing voluntary contractions. Part II-changes in amplitude and spectral characteristics. J Electromyogr Kinesiol 18: 35-43, 2008.
22. Dimitrova NA, Dimitrov V, Nikitin OA. Neither high-pass filtering nor mathematical differentiation of the EMG signals can considerably reduce cross-Talk. J Electromyogr Kinesiol 12: 235-246, 2002.
23. Dimitrova NA, Dimitrov GV. Interpretation of EMG changes with fatigue: Facts, pitfalls, and fallacies. J Electromyogr Kinesiol 13: 13-36, 2003.
24. Evans CM, Baker SN. Task-dependent intermanual coupling of 8-Hz discontinuities during slow finger movements. Eur J Neurosci 18: 453-456, 2003.
25. Enoka RM. Muscle fatigue-from motor units to clinical symptoms. J Biomech 45: 427-433, 2012.
26. Fang Y, Daly JJ, Sun J, Hvorat K, Fredrickson E, Pundik S, Sahgal V, Yue GH. Functional corticomuscular connection during reaching is weakened following stroke. Clin Neurophysiol 120: 994-1002, 2009.
27. Farina D, Rainoldi A. Compensation of the effect of sub-cutaneous tissue layers on surface EMG: A simulation study. Med Eng Phys 21: 487-497, 1999.
28. Farina D, Cescon C, Merletti R. Influence of anatomical, physical and detection-system parameters on surface EMG. Biol Cybern 86: 445-456, 2002.
29. Farina D, Merletti R, Indino B, Nazzaro M, Pozzo M. Cross-Talk between knee extensor muscles. Experimental and model results. Muscle Nerve 26: 681-695, 2002.
30. Farina D, Fosci M, Merletti R. Motor unit recruitment strategies investigated by surface EMG variables. J Appl Physiol 92: 235-247, 2002.
31. Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol 96: 1486-1495, 2004.
32. Farina D, Mesin L, Martina S, Merletti R. A surface EMG generation model with multi-layer cylindrical description of the volume conductor. IEEE Trans Biomed Eng 51: 415-426, 2004.
33. Farina D, Merletti R. Methods for estimating muscle fibre conduction velocity from surface electromyographic signals. Med Biol Eng Comput 42: 432-445, 2004.
34. Farina D. Counterpoint: Spectral properties of the surface EMG do not provide information about motor unit recruitment and muscle fiber type. J Appl Physiol 105: 1673-1674, 2008.
35. Farina D. Last word on point: Counterpoint: Spectral properties of the surface EMG can characterize/do not provide information about motor unit recruitment and muscle fiber type. J Appl Physiol 105: 1683, 2008.
36. Farina D, Cescon C, Negro F, Enoka RM. Amplitude cancellation of motor-unit action potentials in the surface electromyogram can be estimated with spike-Triggered averaging. J Neurophysiol 100: 431-440, 2008.
37. Farina D, Negro F, Gazzoni M, Enoka RM. Detecting the unique representation of motor-unit action potentials in the surface electromyogram. J Neurophysiol 100: 1223-1233, 2008.
38. Farina D, Leclerc F, Arendt-Nielsen L, Buttelli O, Madeleine P. The change in spatial distribution of upper trapezius muscle activity is correlated to contraction duration. J Electromyogr Kinesiol 18: 16-25, 2008.
39. Farina D. Variations in propagation velocity of muscle-fiber action potentials in individual motor units during voluntary contractions. J Appl Physiol 111: 627-629, 2011.
40. Farina D, Enoka RM. Surface EMG decomposition requires an appropriate validation. J Neurophysiol 105: 981-982, 2011.
41. Farina D, Negro F, Jiang N. Identification of common synaptic inputs to motor neurons from the rectified electromyogram. J Physiol 591: 2403-2418, 2013.
42. Farina D, Negro F, Jiang J. Reply from Dario Farina, Francesco Negro and Ning Jiang. J Physiol 592: 251-252, 2014.
43. Farina D, Negro F, Dideriksen JL. The effective neural drive to muscles is the common synaptic input to motor neurons. J Physiol 592: 3427-3441, 2014.
44. Fuglevand AJ, Winter DA, Patla AE. Models of recruitment and rate coding organization in motor unit pools. J Neurophysiol 70: 2470-2488, 1993.
45. Gazzoni M, Farina D, Merletti R. A new method for the extraction and classification of single motor unit action potentials from surface EMG signals. J Neurosci Methods 136: 165-177, 2004.
46. Grosse P, Cassidy MJ, Brown P. EEG-EMG, MEG-EMG and EMGEMG frequency analysis: Physiological principles and clinical applications. Clin Neurophysiol 113: 1523-1531, 2002.
47. 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: 5-8, 1998.
48. Halliday DM, Conway BA, Christensen LO, Hansen NL, Petersen NP, Nielsen JB. Functional coupling of motor units is modulated during walking in human subjects. J Neurophysiol 89: 960-968, 2003.
49. Halliday DM, Farmer SF. On the need for rectification of surface EMG. J Neurophysiol 103: 3547, 2010.
50. Hansen NL, Nielsen JB. The effect of transcranial magnetic stimulation and peripheral nerve stimulation on corticomuscular coherence in humans. J Physiol 561: 295-306, 2004.
51. Holobar A, Zazula D. Multichannel blind source separation using convolution kernel compensation. IEEE Trans Signal Proc 55: 4487-4496, 2007.
52. Holobar A, Farina D, Gazzoni M, Merletti R, Zazula D. Estimating motor unit discharge patterns from high-density surface electromyogram. Clin Neurophysiol 120: 551-562, 2009.
53. Holobar A, Minetto MA, Botter A, Negro F, Farina D. Experimental analysis of accuracy in the identification of motor unit spike trains from high-density surface EMG. IEEE Trans Neural Syst Rehabil Eng 18: 221-229, 2010.
54. Holobar A, Glaser V, Gallego JA, Dideriksen JL, Farina D. Noninvasive characterization of motor unit behaviour in pathological tremor. J Neural Eng 9: 056011, 2012.
55. Holobar A, Minetto M, Farina D. Accurate identification of motor unit discharge patterns from high-density surface EMG and validation with a novel signal-based performance metrics. J Neural Eng 11: 016008, 2014.
56. Holtermann A, Roeleveld K, Karlsson JS. Inhomogeneities in muscle activation reveal motor unit recruitment. J Electromyogr Kinesiol 15: 131-137, 2005.
57. Hu X, Rymer WZ, Suresh NL. Assessment of validity of a high-yield surface electromyogram decomposition. J Neuroeng Rehabil 10: 99, 2013.
58. Hu X, Rymer WZ, Suresh NL. Accuracy assessment of a surface electromyogram decomposition system in human first dorsal interosseus muscle. J Neural Eng 11: 026007, 2014.
59. Jesunathadas M, Aidoor SS, Keenan KG, Farina D, Enoka RM. Influence of amplitude cancellation on the accuracy of determining the onset of muscle activity from the surface electromyogram. J Electromyogr Kinesiol 22: 494-500, 2012.
60. Kilner JM, Baker SN, Lemon RN. A novel algorithm to remove electrical cross-Talk between surface EMG recordings and its application to the measurement of short-Term synchronisation in humans. J Physiol 538: 919-930, 2002.
61. Keenan KG, Farina D, Maluf KS, Merletti R, Enoka RM. Influence of amplitude cancellation on the simulated surface electromyogram. J Appl Physiol 98: 120-131, 2005.
62. Keenan KG, Farina D, Merletti R, Enoka RM. Amplitude cancellation reduces the size of motor unit potentials averaged from the surface EMG. J Appl Physiol 100: 1928-1937, 2006.
63. Keenan KG, Farina D, Meyer FG, Merletti R, Enoka RM. Sensitivity of the cross-correlation between simulated surface EMGs for two muscles to detect motor unit synchronization. J Appl Physiol 102: 1193-1201, 2007.
64. Kleine BU, Schumann NP, Stegeman DF, Scholle HC. Surface EMG mapping of the human trapezius muscle: The topography of monopolar and bipolar surface EMG amplitude and spectrum parameters at varied forces and in fatigue. Clin Neurophysiol 111: 686-693, 2000.
65. Kleine BU, van Dijk JP, Lapatki BG, Zwarts MJ, Stegeman DF. Using two-dimensional spatial information in decomposition of surface EMG signals. J Electromyogr Kinesiol 17: 535-548, 2007.
66. Knaflitz M, Bonato P. Time-frequency methods applied to muscle fatigue assessment during dynamic contractions. J Electromyogr Kinesiol 9: 337-350, 1999.
67. Lapatki BG, Oostenveld R, Van Dijk JP, Jonas IE, Zwarts MJ, Stegeman DF. Topographical characteristics of motor units of the lower facial musculature revealed by means of high-density surface EMG. J Neurophysiol 95: 342-354, 2006.
68. Li X, Holobar A, Gazzoni M, Botter A, Merletti R, Rymer WZ, Zhou P. Post stroke motor unit firing rate alteration examined by high density surface electromyography decomposition (Abstract). Neuroscience 338.10/V2, 2013.
69. Lindstrom L, Magnusson R. Interpretation of myoelectric power spectra: A model and its applications. Proc IEEE 65: 653-662, 1977.
70. Lowery MM, Stoykov NS, Kuiken TA. A simulation study to examine the use of cross-correlation as an estimate of surface EMG cross talk. J Appl Physiol 94: 1324-1334, 2003.
71. Mambrito B, De Luca CJ. A technique for the detection, decomposition and analysis of the EMG signal. Electroencephalogr Clin Neurophysiol 58: 175-188, 1984.
72. Marateb HR, McGill KC, Holobar A, Lateva ZC, Mansourian M, Merletti R. Accuracy assessment of CKC high-density surface EMG decomposition in biceps femoris muscle. J Neural Eng 8: 066002, 2011.
73. Mathiassen SE, Winkel J, Hägg GM. Normalization of surface EMG amplitude from the upper trapezius muscle in ergonomic studies-A review. J Electromyogr Kinesiol 5: 197-226, 1995.
74. McClelland VM, Cvetkovic Z, Mills KR. Rectification of the EMG is an unnecessary and inappropriate step in the calculation of Corticomuscular coherence. J Neurosci Methods 205: 190-201, 2012.
75. McClelland VM, Cvetkovic Z, Mills KR. Inconsistent effects of EMG rectification on coherence analysis. J Physiol 592: 249-250, 2014.
76. McGill KC, Lateva ZC, Marateb HR. EMGLAB: An interactive EMG decomposition program. J Neurosci Methods 149: 121-133, 2005.
77. McGill KC, Lateva ZC. History dependence of human muscle-fiber conduction velocity during voluntary isometric contractions. J Appl Physiol 111: 630-641, 2011.
78. Mottram CJ, Jakobi JM, Semmler JG, Enoka RM. Motor-unit activity differs with load type during a fatiguing contraction. J Neurophysiol 93: 1381-1392, 2005.
79. Myers LJ, Lowery M, O'Malley M, Vaughan CL, Heneghan C, St Clair Gibson A, Harley YX, Sreenivasan R. Rectification and nonlinear pre-processing of EMG signals for cortico-muscular analysis. J Neurosci Methods 124: 157-165, 2003.
80. Nakao M, Norimatsu M, Mizutani Y, Yamamoto M. Spectral distortion properties of the integral pulse frequency modulation model. IEEE Trans Biomed Eng 44: 419-426, 1997.
81. Nawab SH, Chang SS, De Luca CJ. High-yield decomposition of surface EMG signals. Clin Neurophysiol 121: 1602-1615, 2010.
82. Negro F, Farina D. Linear transmission of cortical oscillations to the neural drive to muscles is mediated by common projections to populations of motoneurons in humans. J Physiol 589: 629-637, 2011.
83. Negro F, Farina D. Decorrelation of cortical inputs and motoneuron output. J Neurophysiol 106: 2688-2697, 2011.
84. Negro F, Farina D. Factors influencing the estimates of correlation between motor unit activities in humans. PLoS One 7: E44894, 2012.
85. Negro F, Holobar A, Farina D. Fluctuations in isometric muscle force can be described by one linear projection of low-frequency components of motor unit discharge rates. J Physiol 587: 5925-5938, 2009.
86. Nielsen JB, Brittain JS, Halliday DM, Marchand-Pauvert V, Mazevet D, Conway BA. Reduction of common motoneuronal drive on the affected side during walking in hemiplegic stroke patients. Clin Neurophysiol 119: 2813-2818, 2008.
87. Pfurtscheller G, Lopes da Silva FH. Event-related EEG/MEG synchronization and desynchronization: Basic principles. Clin Neurophysiol 110: 1842-1857, 1999.
88. Pohja M, Salenius S. Modulation of cortex-muscle oscillatory interaction by ischaemia-induced deafferentation. Neuroreport 14: 321-324, 2003.
89. Qi L, Wakeling JM, Green A, Lambrecht K, Ferguson-Pell M. Spectral properties of electromyographic and mechanomyographic signals during isometric ramp and step contractions in biceps brachii. J Electromyogr Kinesiol 21: 128-135, 2011.
90. Riddle CN, Baker SN. Manipulation of peripheral neural feedback loops alters human corticomuscular coherence. J Physiol 566: 625-639, 2005.
91. Roy SH, De Luca CJ, Schneider J. Effects of electrode location on myoelectric conduction velocity and median frequency estimates. J Appl Physiol 61: 1510-1517, 1986.
92. Salenius S, Portin K, Kajola M, Salmelin R, Hari R. Cortical control of human motoneuron firing during isometric contraction. J Neurophysiol 77: 3401-3405, 1997.
93. Salenius S, Avikainen S, Kaakkola S, Hari R, Brown P. Defective cortical drive to muscle in Parkinson's disease and its improvement with levodopa. Brain 125: 491-500, 2002.
94. Solomonow M, Baten C, Smith J, Baratta R, Hermens H, D'Ambrosia R, Shoji H. Electromyogram power spectra frequencies associated with motor unit recruitment strategies. J Appl Physiol 68: 1177-1185, 1990.
95. Stalberg E. Propagation velocity in human muscle fibers in situ. Acta Physiol Scand Suppl 287: 1-112, 1966.
96. Staudenmann D, Kingma I, Daffertshofer A, Stegeman DF, van Dieën JH. Improving EMG-based muscle force estimation by using a high-density EMG grid and principal component analysis. IEEE Trans Biomed Eng 53: 712-719, 2006.
97. Staudenmann D, van Dieën JH, Stegeman DF, Enoka RM. Increase in heterogeneity of biceps brachii activation during isometric submaximal fatiguing contractions: A multichannel surface EMG study. J Neurophysiol 111: 984-990, 2014.
98. Strens LH, Asselman P, Pogosyan A, Loukas C, Thompson AJ, Brown P. Corticocortical coupling in chronic stroke: Its relevance to recovery. Neurology 63: 475-484, 2004.
99. Tecchio F, Porcaro C, Zappasodi F, Pesenti A, Ercolani M, Rossini PM. Cortical short-Term fatigue effects assessed via rhythmic brainmuscle coherence. Exp Brain Res 174: 144-151, 2006.
100. Troni W, Cantello R, Rainero I. Conduction velocity along human muscle fibers in situ. Neurology 33: 1453-1459, 1983.
101. Vieira TM, Loram ID, Muceli S, Merletti R, Farina D. Postural activation of the human medial gastrocnemius muscle: Are the muscle units spatially localised? J Physiol 589: 431-443, 2011.
102. von Tscharner V, Nigg BM. Point: Spectral properties of the surface EMG can characterize/do not provide information about motor unit recruitment strategies and muscle fiber type. J Appl Physiol 105: 1671-1673, 2008.
103. von Tscharner V, Nigg BM. Last word on point: Counterpoint: Spectral properties of the surface EMG can characterize/do not provide information about motor unit recruitment strategies and muscle fiber type. J Appl Physiol 105: 1682, 2008.
104. Volkmann J, Joliot M, Mogilner A, Ioannides AA, Lado F, Fazzini E, Ribary U, Llinas R. Central motor loop oscillations in parkinsonian resting tremor revealed by magnetoencephalography. Neurology 46: 1359-1370, 1996.
105. Ward NJ, Farmer SF, Berthouze L, Halliday DM. Rectification of EMG in low force contractions improves detection of motor unit coherence in the beta-frequency band. J Neurophysiol 110: 1744-1750, 2013.
106. Yang Q, Fang Y, Sun CK, Siemionow V, Ranganathan VK, Khoshknabi D, Davis MP, Walsh D, Sahgal V, Yue GH. Weakening of functional corticomuscular coupling during muscle fatigue. Brain Res 1250: 101-112, 2009.