Training adaptations in the behavior of human motor units

Journal of Applied Physiology

Volumn 101, Issue 6, 2006, Pages 1766-1775

  Duchateau, Jacques ^a   Semmler, John G ^b   Enoka, Roger M ^c  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Discharge rate; Electromyogram; Motor unit synchronization; Recruitment; Steadiness

Indexed keywords

ADAPTATION; DAILY LIFE ACTIVITY; ELECTROMYOGRAPHY; EVOKED RESPONSE; FEEDBACK SYSTEM; HUMAN; MOTONEURON; MOTOR COORDINATION; MOTOR PERFORMANCE; MOTOR UNIT; MOTOR UNIT POTENTIAL; MUSCLE CONTRACTION; MUSCLE FORCE; MUSCLE STRENGTH; PRIORITY JOURNAL; REVIEW; SENSORY NERVE; SPINAL CORD; TORQUE; TRAINING;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; EXERCISE; HUMANS; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE FIBERS; MUSCLE, SKELETAL; PHYSICAL FITNESS;

EID: 33750834574     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00543.2006     Document Type: Review

References (148)

1. Aagaard P, Simonsen EB, Andersen JL, Magnusson P, and Dyhre-Poulsen P. Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 92: 2309-2318, 2002.
2. Aagaard P, Simonsen EB, Andersen JL, Magnusson SP, Halkjaer-Kristensen J, and Dyhre-Poulsen P. Neural inhibition during maximal eccentric and concentric quadriceps contraction: effects of resistance training. J Appl Physiol 89: 2249-2257, 2000.
3. Adrian E and Bronk D. The discharge of impulses in motor nerve fibres. II. The frequency of discharges in reflex and voluntary contractions. J Physiol 204: 231-257, 1929.
4. Allen GM, Gandevia SC, and McKenzie DK. Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18: 593-600, 1995.
5. Amiridis IG, Martin A, Morlon B, Martin L, Cometti G, Pousson M, and van Hoecke J. Co-activation and tension-regulating phenomena during isokinetic knee extension in sedentary and highly skilled humans. Eur J Appl Physiol 73: 149-156, 1996.
6. Bakels R and Kernell D. Matching between motoneurone and muscle unit properties in rat medial gastrocnemius. J Physiol 463: 307-324, 1993.
7. Baratta R, Solomonow M, Zhou BH, Letson D, Chuinard R, and D'Ambrosia R. Muscular coactivation. The role of the antagonist musculature in maintaining knee stability. Am J Sports Med 16: 113-122, 1988.
8. Barry BK, Riek S, and Carson RG. Muscle coordination during rapid force production by young and older adults. J Gerontol 60A: 232-240, 2005.
9. Beaumont E and Gardiner PF. Endurance training alters the biophysical properties of hindlimb motoneurons in rats. Muscle Nerve 27: 228-236, 2003.
10. Belanger AY and McComas AJ. Extent of motor unit activation during effort. J Appl Physiol 51: 1131-1135, 1981.
11. Bellemare F, Woods JJ, Johansson R, and Bigland-Ritchie B. Motor-unit discharge rates in maximal voluntary contractions of three human muscles. J Neurophysiol 50: 1380-1392, 1983.
12. Binder MD, Heckman CJ, and Powers RK. The physiological control of motoneuron activity. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, chapt. 1, p. 1-53.
13. Burke RE, Jankowska E, and Ten Bruggencate G. A comparison of peripheral and rubrospinal synaptic input to slow and fast twitch motor units of triceps surae. J Physiol 207: 709-732, 1970.
14. Burke RE, Levine DN, Tsairis P, and Zajac FE. Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol 234: 723-748, 1973.
15. Burke RE, Strick PL, Kanda K, Kim CC, and Walmsley B. Anatomy of medial gastrocnemius and soleus motor nuclei in cat spinal cord. J Neurophysiol 40: 667-680, 1977.
16. Burnett RA, Laidlaw DH, and Enoka RM. Coactivation of the antagonist muscle does not covary with steadiness in old adults. J Appl Physiol 89: 61-71, 2000.
17. Calancie B and Bawa P. Firing patterns of human flexor carpi radialis motor units during the stretch reflex. J Neurophysiol 53: 1179-1193, 1985.
18. Carolan B and Cafarelli E. Adaptations in coactivation after isometric resistance training. J Appl Physiol 73: 911-917, 1992.
19. Carroll TJ, Riek S, and Carson RG. Corticospinal responses to motor training revealed by transcranial magnetic stimulation. Exerc Sport Sci Rev 29: 54-59, 2001.
20. Carroll TJ, Riek S, and Carson RG. The sites of neural adaptation induced by resistance training in humans. J Physiol 544: 641-652, 2002.
21. Christou EA, Grossman M, and Carlton LG. Modeling variability of force during isometric quadriceps femoris muscle contractions. J Mot Behav 34: 67-81, 2002.
22. Christou EA, Zelent M, and Carlton LG. Force control is greater in upper compared with the lower extremity. J Mot Behav 35: 322-324, 2003.
23. Christou EA, Jakobi JM, Critchlow A, Fleshner M, and Enoka RM. The 1-2 Hz oscillations in muscle force are exacerbated by stress, especially in older adults. J Appl Physiol 97: 225-235, 2004.
24. Classen J, Liepert J, Wise SP, Hallet M, and Cohen LG. Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79: 1117-1123, 1998.
25. Connelly DM, Rice CL, Roos MR, and Vandervoort AA. Motor unit firing rates and contractile properties in tibialis anterior of young and old men. J Appl Physiol 87: 843-852, 1999.
26. Cracraft JD and Petajan JH. Effect of muscle training on the pattern of firing of single motor units. Am J Phys Med 56: 183-194, 1977.
27. Datta AK and Stephens JA. Synchronization of motor unit activity during voluntary contraction in man. J Physiol 422: 397-419, 1990.
28. Davies CTM, Dooley P, McDonagh MJN, and White MJ. Adaptation of mechanical properties of muscle to high force training in man. J Physiol 365: 277-284, 1985.
29. Day SJ and Hulliger M. Experimental simulation of cat electromyogram: evidence for algebraic summation of motor-unit action-potential trains. J Neurophysiol 86: 2144-2158, 2001.
30. De Luca CJ and Erim Z. Common drive of motor units in regulation of muscle force. Trends Neurosci 17: 299-305, 1994.
31. De Luca CJ and Mambrito B. Voluntary control of motor units in human antagonist muscles: coactivation and reciprocal activation. J Neurophysiol 58: 525-542, 1987.
32. De Luca CJ, LeFever RS, McCue MP, and Xenakis AP. Behavior of human motor units in different muscles during linearly varying contractions. J Physiol 329: 113-128, 1982.
33. Desmedt JE and Godaux E. Ballistic contractions in man: characteristic recruitment pattern of single motor units of the tibialis anterior muscle. J Physiol 264: 673-693, 1977.
34. Desmedt JE and Godaux E. Ballistic contractions in fast or slow human muscles: discharge patterns of single motor units. J Physiol 285: 185-196, 1978.
35. Duchateau J and Hainaut K. Training effects of sub-maximal electrostimulation in a human muscle. Med Sci Sports Exerc 20: 99-104, 1988.
36. Duchateau J and Hainaut K. Effects of immobilization on contractile properties, recruitment and firing rates of human motor units. J Physiol 422: 55-65, 1990.
37. Enoka RM and Fuglevand AJ. Motor unit physiology: some unresolved issues. Muscle Nerve 24: 4-17, 2001.
38. Enoka RM, Robinson GA, and Kossev AR. Task and fatigue effects on low-threshold motor units in human hand muscle. J Neurophysiol 62: 1344-1359, 1989.
39. Enoka RM, Christou EA, Hunter SK, Kornatz KW, Semmler JG, Taylor AM, and Tracy BL. Mechanisms that contribute to differences in motor performance between young and old adults. J Electromyogr Kinesiol 13: 1-12, 2003.
40. Erim Z, De Luca CJ, Mineo K, and Aoki T. Rank-ordered regulation of motor units. Muscle Nerve 19: 563-573, 1996.
41. Farina D, Merletti R, and Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol 96: 1486-1495, 2004.
42. Farmer SF, Swash M, Ingram DA, and Stephens JA. Changes in motor unit synchronization following central nervous lesions in man. J Physiol 463: 83-105, 1993.
43. Farmer SF, Bremner FD, Halliday DM, Rosenberg JR, and Stephens JA. The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. J Physiol 470: 127-155, 1993.
44. Feiereisen P, Duchateau J, and Hainaut K. Motor unit recruitment order during voluntary and electrically induced contractions in the tibialis anterior. Exp Brain Res 114: 117-123, 1997.
45. Freund HJ, Büdingen HJ, and Dietz V. Activity of single motor units from human forearm muscles during voluntary isometric contraction. J Neurophysiol 38: 933-946, 1975.
46. Fuglevand AJ, Winter DA, and Patla AE. Models of recruitment and rate coding organization in motor-unit pools. J Neurophysiol 70: 2470-2488, 1993.
47. Galganski ME, Fuglevand AJ, and Enoka RM. Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. J Neurophysiol 69: 2108-2115, 1993.
48. Gandevia SC, Herbert RD, and Leeper JB. Voluntary activation of human elbow flexor muscles during maximal concentric contractions. J Physiol 512: 595-602, 1998.
49. Gardiner PF. Changes in α-motoneuron properties with altered physical activity levels. Exerc Sport Sci Rev 34: 54-58, 2006.
50. Gorassini M, Yang JF, Siu M, and Bennett DJ. Intrinsic activation of human motoneurons: reduction of motor unit recruitment thresholds by repeated contractions. J Neurophysiol 87: 1859-1866, 2002.
51. Graves AE, Kornatz KW, and Enoka RM. Older adults use a unique strategy to lift inertial loads with the elbow flexor muscles. J Neurophysiol 83: 2030-2039, 2000.
52. Gydikov A and Kosarov D. Some features of different motor units in human biceps brachii. Pflügers Arch 347: 75-88, 1974.
53. Hainaut K, Duchateau J, and Desmedt JE. Differential effects of slow and fast motor units of different programs of brief daily muscle training in man. In: New Developments in Electromyography and Clinical Neurophysiology. Basel: Karger, 1981, vol. 9, p. 241-249.
54. Häkkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Mälkiä E, Kraemer WJ, Newton RU, and Alen M. Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol 84: 1341-1349, 1998.
55. Harridge SDR, Kryger A, and Stensgaard A. Knee extensor strength, activation, and size in very elderly people following strength training. Muscle Nerve 22: 831-839, 1999.
56. Harris CM and Wolpert DM. Signal-dependent noise determines motor planning. Nature 394: 780-784, 1998.
57. Heckman CJ and Enoka RM. Physiology of the motor neuron and the motor unit. In: Clinical Neurophysiology of Motor Neuron Diseases. Handbook of Clinical Neurophysiology, edited by Eisen A. New York: Elsevier, 2004, vol. 4, p. 119-147.
58. Heckman CJ, Lee RH, and Brownstone RM. Hyperexcitable dendrites in motoneurons and their neuromodulatory control during motor behavior. Trends Neurosci 26: 688-695, 2003.
59. Henneman E. Relation between size of neurons and their susceptibility to discharge. Science 126: 1345-1347, 1957.
60. Ivanova T, Garland SJ, and Miller KJ. Motor unit recruitment and discharge behavior in movements and isometric contractions. Muscle Nerve 20: 867-874, 1997.
61. Jensen JL, Marstrand PC, and Nielsen JB. Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol 99: 1558-1568, 2005.
62. Kakuda N, Nagaoka M, and Wessberg J. Common modulation of motor unit pairs during slow wrist movement in man. J Physiol 520: 929-940, 1999.
63. Kamen G and Knight CA. Training-related adaptations in motor unit discharge rate in young and older adults. J Gerontol A Biol Sci Med Sci 59: 1334-1338, 2004.
64. Keen DA, Yue GH, and Enoka RM. Training-related enhancement in the control of motor unit output in elderly humans. J Appl Physiol 77: 2648-2658, 1994.
65. Keenan KG, Farina D, Maluf KS, Merletti R, and Enoka RM. Influence of amplitude cancellation on the simulated surface electromyogram. J Appl Physiol 98: 120-131, 2005.
66. Kellis E. Quantification of quadriceps and hamstring antagonist activatity. Sports Med 25: 37-62, 1998.
67. Kent-Braun JA and Le Blanc R. Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 19: 861-869, 1996.
68. Kernell D. The adaptation and the relation between discharge frequency and current strength of cat lumbo-sacral motoneurones stimulated by long-lasting injected currents. Acta Physiol Scand 65: 65-73, 1965.
69. Kernell D. Input resistance, electrical excitability, and size of ventral horn cells in cat spinal cord. Science 152: 1637-1640, 1966.
70. Kernell D, Eerbeek O, and Verhey BA. Motor unit categorization on basis of contractile properties: an experimental analysis of the composition of the cat's m. peroneus longus. Exp Brain Res 50: 211-219, 1983.
71. Klass M, Baudry S, and Duchateau J. Contractile properties of single motor units in elderly. Comp Meth Biomech Biomed Eng 1, Suppl: 167-168, 2005.
72. Knight CA and Kamen G. Adaptations in muscular activation of the knee extensor muscles with strength training in young and older adults. J Electromyogr Kinesiol 11: 405-412, 2001.
73. Knight CA and Kamen G. Enhanced motor unit rate coding with improvements in a force-matching task. J Electromyogr Kinesiol 14: 619-629, 2004.
74. Kornatz KW, Christou EA, and Enoka RM. Practice reduces motor unit discharge variability in a hand muscle and improves manual dexterity in old adults. J Appl Physiol 98: 2072-2080, 2005.
75. Kukulka CG and Clamann HP. 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, 1981.
76. Laidlaw DH, Bilodeau M, and Enoka RM. Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve 23: 600-612, 2000.
77. Le Bozec S and Bouisset S. Does postural chain mobility influence muscular control in sitting ramp pushes? Exp Brain Res 158: 427-437, 2004.
78. LeFever RS and De Luca CJ. A procedure for decomposing the myoelectric signal into its constituent action potentials. I. Technique, theory, and implementation. IEEE Trans Biomed Eng 29: 149-157, 1982.
79. Leong B, Kamen G, Patten C, and Burke JR. Maximal motor unit discharge rates in the quadriceps muscles of older weight lifters. Med Sci Sports Exerc 31: 1638-1644, 1999.
80. Lévénez M, Kotzamanidis C, Carpentier A, and Duchateau J. Spinal reflexes and coactivation of ankle muscles during a submaximal fatiguing contraction. J Appl Physiol 99: 1182-1188, 2005.
81. Liepert J, Classen J, Cohen LG, and Hallett M. Task-dependent changes of intracortical inhibition. Exp Brain Res 118: 421-426, 1998.
82. Macefield VG, Gandevia SC, Bigland-Ritchie B, Gorman RB, and Burke D. The firing rates of human motoneurones voluntarily activated in the absence of muscle afferent feedback. J Physiol 471: 429-443, 1993.
83. Macefield VG, Fuglevand AJ, and Bigland-Ritchie B. Contractile properties of single motor units in human toe extensors assessed by intraneural motor axon stimulation. J Neurophysiol 75: 2509-2519, 1996.
84. Merletti R and Parker PA (Editors). Electromyography: Physiology, Engineering, and Noninvasive Applications. Hoboken, NJ: Wiley, 2004.
85. Merletti R, Rainoldi A, and Farina D. Surface electromyography for noninvasive characterization of muscle. Exerc Sport Sci Rev 29: 20-25, 2001.
86. Merton PA. Voluntary strength and fatigue. J Physiol 123: 553-564, 1954.
87. Miller RG, Mirka A, and Maxfield M. Rate of tension development in isometric contractions of a human hand muscle. Exp Neurol 73: 267-285, 1981.
88. Milner-Brown HS, Stein RB, and Lee RG. Synchronization of human motor units: possible roles of exercise and supraspinal reflexes. Electroencephalogr Clin Neurophysiol 38: 245-254, 1975.
89. Milner-Brown HS, Stein RB, and Yemm R. The orderly recruitment of human motor units during voluntary isometric contractions. J Physiol 230: 359-370, 1973.
90. Monster AW and Chan J. Isometric force production by motor units of extensor digitorum communis in man. J Neurophysiol 40: 1432-1443, 1977.
91. Moritani T and deVries HA. Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 58: 115-130, 1979.
92. Moritz CT, Barry BK, Pascoe MA, and 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.
93. Mottram CJ, Christou EA, Meyer FG, and Enoka RM. Frequency modulation of motor unit discharge has task-dependent effects on fluctuations in motor output. J Neurophysiol 94: 2878-2887, 2005.
94. Mottram CJ, Jakobi JM, Semmler JG, and Enoka RM. Motor unit activity differs with load type during fatiguing contraction. J Neurophysiol 93: 1381-1393, 2005.
95. Munn J, Herbert RD, Hancock MJ, and Gandevia SC. Training with unilateral resistance exercise increases contralateral strength. J Appl Physiol 99: 1880-1884, 2005.
96. Nielsen JB. Sensorimotor integration at spinal level as a basis for muscle coordination during voluntary movement in humans. J Appl Physiol 96: 1961-1967, 2004.
97. Pascual-Leone A, Dang N, Cohen LG, Brasil-Neto JP, Cammarota A, and Hallett M. Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74: 1037-1045, 1995.
98. Pasquet B, Carpentier A, and Duchateau J. Change in muscle fascicle length influences the recruitment and discharge rate of motor units during isometric contractions. J Neurophysiol 94: 3126-3133, 2005.
99. Patten C and Kamen G. Adaptations in motor unit discharge activity with force control training in young and older human adults. Eur J Appl Physiol 83: 128-143, 2000.
100. Patten C, Kamen G, and Rowland DM. Adaptations in maximal motor unit discharge rate to strength training in young and older adults. Muscle Nerve 24: 542-550, 2001.
101. Person RS and Kudina LP. Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle. Electroencephalogr Clin Neurophysiol 32: 471-483, 1972.
102. Pinninger GJ, Steele JR, Thorstensson A, and Cresswell AG. Tension regulation during lengthening and shortening actions of the human soleus muscle. Eur J Appl Physiol 81: 375-383, 2000.
103. Ploutz LL, Tesch PA, Biro RL, and Dudley GA. Effect of resistance training on muscle use during exercise. J Appl Physiol 7: 1675-1681, 1994.
104. Psek JA and Cafarelli E. Behavior of coactive muscles during fatigue. J Appl Physiol 74: 170-175, 1993.
105. Pucci AR, Griffin L, and Cafarelli E. Maximal motor unit firing rates during isometric resistance training in men. Exp Physiol 91: 171-178, 2005.
106. Rich C and Cafarelli E. Submaximal motor unit firing rates after 8 wk of isometric resistance training. Med Sci Sports Exerc 32: 190-196, 2000.
107. Rothwell JC. Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Methods 74: 113-122, 1997.
108. Rudroff T, Poston B, Shin IS, Bojsen-Møller J, and Enoka RM. Net excitation of the motor unit pool varied with load type during fatiguing contractions. Muscle Nerve 29: 78-87, 2005.
109. Rutherford OM and Jones DA. The role of learning and coordination in strength training. Eur J Appl Physiol 55: 100-105, 1986.
110. Sale DG. Neural adaptation to resistance training. Med Sci Sports Exerc 20, Suppl: S135-S145, 1988.
111. Sale DG, MacDougall JD, Upton ARM, and McComas AJ. Effect of strength training upon motoneuron excitability in man. Med Sci Sports Exerc 125: 57-62, 1983.
112. Scaglioni G, Ferri A, Minetti AE, Martin A, Van Hoecke J, Capodaglio P, Sartorio A, and Narici MV. Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training. J Appl Physiol 92: 2292-2302, 2002.
113. Schmidt RA, Zelaznik H, Hawkins B, Frank JS, and Quinn JT Jr. Motor-output variability: a theory for the accuracy of rapid motor acts. Psychol Rev 47: 415-451, 1979.
114. Schwindt PC. Membrane-potential trajectories underlying motoneuron rhythmic firing at high rates. J Neurophysiol 36: 434-439, 1973.
115. Sears TA and Stagg D. Short-term synchronization of intercostals motoneurone activity. J Physiol 263: 357-381, 1976.
116. Semmler JG. Motor unit synchronization and neuromuscular performance. Exerc Sport Sci Rev 30: 8-14, 2002.
117. Semmler JG and Enoka RM. Neural contributions to changes in muscle strength. In: Biomechanics in Sport: Performance Enhancement and Injury Prevention, edited by Zatsiorsky VM. Oxford, UK: Blackwell Science, 2000, p. 3-20.
118. Semmler JG and Nordstrom MA. Motor unit discharge and force tremor in skill- and strength-trained individuals. Exp Brain Res 119: 27-38, 1998.
119. Semmler JG, Kornatz KW, and Enoka RM. Motor-unit coherence during isometric contractions is greater in a hand muscle of older adults. J Neurophysiol 90: 1346-1349, 2003.
120. Semmler JG, Sale MV, and Kidgell DJ. Motor unit synchronization measured by cross-correlation is not increased with strength training of a hand muscle. Proc Int Australas Winter Conf Brain Res 24: 2-5, 2006.
121. Semmler JG, Sale MV, Meyer FG, and Nordstrom MA. Motor-unit coherence and its relation with synchrony are influenced by training. J Neurophysiol 92: 3320-3331, 2004.
122. Semmler JG, Kornatz KW, Dinenno DV, Zhou S, and Enoka RM. Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle. J Physiol 545: 681-695, 2002.
123. Shemmell J, Tresilian JR, Riek S, Barry BK, and Carson RG. Neuromuscular adaptation during skill acquisition on a two-degree-of-freedom target-acquisition task: dynamic movement. J Neurophysiol 94: 3058-3068, 2005.
124. Sherrington C. Remarks on some aspects of reflex inhibition. Proc R Soc Lond B Biol Sci B97: 19-45, 1925.
125. Slifkin AB and Newell KM. Noise, information transmission, and force variability. J Exp Psychol 25: 837-851, 1999.
126. Sogaard K, Christensen H, Jensen BR, Finsen L, and Sjogaard G. Motor control and kinetics during low level concentric and eccentric contractions in man. Electroencephalogr Clin Neurophysiol 101: 453-460, 1996.
127. Spiegel KM, Stratton J, Burke JR, Glendinning DS, and Enoka RM. The influence of age on the assessment of motor unit activation in a human hand muscle. Exp Physiol 81: 805-819, 1996.
128. Stalberg E. Macro EMG, a new recording technique. J Neurol Neurosurg Psychiatry 43: 475-482, 1980.
129. Stalberg E, Nandedkar SD, Sanders DB, and Falck B. Quantitative motor unit potential analysis. J Clin Neurophysiol 13: 401-422, 1996.
130. Stevens JE, Stackhouse SK, Binder-Macleod SA, and Snyder-Mackler L. Are voluntary muscle activation deficits in older adults meaningful? Muscle Nerve 27: 99-101, 2003.
131. Stotz PJ and Bawa P. Motor unit recruitment during lengthening contractions of human wrist flexors. Muscle Nerve 24: 1535-1541, 2001.
132. Tanji J and Kato M. Recruitment of motor units in voluntary contraction of a finger muscle in man. Exp Neurol 40: 759-770, 1973.
133. Tax AA, Denier van der Gon JJ, Gielen CC, and van den Tempel CM. Differences in the activation of m. biceps brachii in the control of slow isotonic movements and isometric contractions. Exp Brain Res 76: 55-63, 1989.
134. Taylor AM, Christou EA, and Enoka RM. Multiple features of motor-unit activity influence force fluctuations during isometric contractions. J Neurophysiol 90: 1350-1361, 2003.
135. Thomas CK, Ross BH, and Stein RB. Motor-unit recruitment in human first dorsal interosseus muscle for static contractions in three different directions. J Neurophysiol 55: 1017-1029, 1986.
136. Todd G, Taylor JL, and Gandevia SC. Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J Physiol 551: 661-671, 2003.
137. Vaillancourt DE, Larsson L, and Newell KM. Effects of aging on force variability, single motor unit discharge patterns, and the structure of 10, 20, and 40 Hz EMG activity. Neurobiol Aging 24: 25-35, 2003.
138. Vallbo ÅB and Wessberg J. Organization of motor output in slow finger movements in man. J Physiol 469: 673-691, 1993.
139. Van Cutsem M and Duchateau J. Preceding muscle activity influences motor unit discharge and rate of torque development during ballistic contractions in humans. J Physiol 562: 635-644, 2005.
140. Van Cutsem M, Duchateau J, and Hainaut K. Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans. J Physiol 513: 295-305, 1998.
141. Van Cutsem M, Feiereisen P, Duchateau J, and Hainaut K. Mechanical properties and behaviour of motor units in the tibialis anterior during voluntary contractions. Can J Appl Physiol 22: 585-597, 1997.
142. Westing SH, Seger JY, and Thorstensson A. Effects of electrical stimulation on eccentric and concentric torque-velocity relationships during knee extension in man. Acta Physiol Scand 140: 17-22, 1990.
143. Wilson GJ, Murphy AJ, and Walshe A. The specificity of strength training: the effect of posture. Eur J Appl Physiol 73: 346-352, 1996.
144. Wolpaw JR, Maniccia DM, and Elia T. Operant conditioning of primate H-reflex: phases of development. Neurosci Lett 170: 203-207, 1994.
145. Yao W, Fuglevand AJ, and Enoka RM. Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions. J Neurophysiol 83: 441-452, 2000.
146. Yue G, Fuglevand AJ, Nordstrom MA, and Enoka RM. Limitations of the surface electromyography technique for estimating motor unit synchronization. Biol Cybern 73: 223-233, 1995.
147. Zehr PE. Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86: 455-468, 2002.
148. Zoghi M, Pearce SL, and Nordstrom MA. Differential modulation of intracortical inhibition in human motor cortex during selective activation of an intrinsic hand muscle. J Physiol 550: 933-946, 2003.