Neural adaptations with chronic physical activity

Journal of Biomechanics

Volumn 30, Issue 5, 1997, Pages 447-455

  Enoka, Roger M ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; MUSCLE;

CHRONIC PHYSICAL ACTIVITY; MOTOR NEURONS;

NEUROPHYSIOLOGY;

ADAPTATION; HOFFMANN REFLEX; HUMAN; MOTONEURON; MUSCLE EXCITATION; NEUROMUSCULAR FUNCTION; PHYSICAL ACTIVITY; PRIORITY JOURNAL; REVIEW; TRAINING;

EID: 0031149044     PISSN: 00219290     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0021-9290(96)00170-4     Document Type: Article

References (116)

1. Abbruzzese, G., Morena, M., Spadavecchia, L. and Schieppati, M. (1994) Response of arm flexor muscles to magnetic stimulation and electrical brain stimulation during shortening and lengthening tasks in man. J. Physiol. (Lond.) 481, 499-507
2. Adams, G. R., Harris, R. T., Woodard, D. and Dudley, G. (1993) Mapping of electrical muscle stimulation using MRI. J. appl. Physiol. 74, 532-537.
3. Allen, G. M., Gandevia, S. C. and McKenzie, D. K. (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18, 593-600.
4. Amiridis, I. G., Martin, A., Morlon, B., Martin, L., Cometti, G., Pousson, M. and van Hoecke, J. (1996) Co-activation and tension-regulating phenomena during isokinetic knee extension in sedentary and highly skilled humans. Eur. J. Appl. Physiol. 73, 149-156.
5. Baldissera, F., Cavallari, P. and Dworzak, F. (1994) Motor neuron 'bistability'. A pathogenic mechanism for cramps and myokymia, Brain 117, 929-939.
6. Behm, D. G. and Sale, D. G. (1993) Intended rather than actual movement velocity determines velocity-specific training response. J. appl. Physiol. 74, 359-368.
7. Belanger, A. Y. and McComas, A. J. (1981) Extent of motor unit activation during effort. J. appl. Physiol. 51, 381-393.
8. Bellemare, F., Woods, J. J., Johansson, R. S. and Bigland-Ritchie, B. (1983) Motor-unit discharge rates during maximal voluntary contractions of three human muscle. J. Neurophysiol. 50, 1380-1392.
9. Bremner, F. D., Bake, J. R. and Stephens, J. A. (1991) Effect of task on the degree of synchronization of intrinsic hand muscle motor units in man. J. Neurophysiol. 66, 2072-2083.
10. Brooks, S. V. and Faulkner, J. A. (1988) Contractile properties of skeletal muscles from young, adult, and aged mice. J. Physiol. (Lond.) 404, 71-82.
11. Brouwer, B. and Qiao, J. (1995) Characteristics and variability of lower limb motoneuron responses to transcranial magnetic stimulation. Electroenceph. Clin. Neurophysiol. 97, 49-54.
12. Caiozzo, V. J., Perrine, J. J. and Edgerton, V. R. (1981) Training-induced alterations in the in-vivo force velocity relationship of human muscle. J. Appl. Physiol. 51, 750-754.
13. Campbell, M. J., McComas, A. J. and Petito, F. (1973) Physiological changes in ageing muscle. J. Neurol. Neurosurg. Psychiat. 36, 174-182.
14. Cannon, R. J. and Cafarelli, E. (1987) Neuromuscular adaptations to training. J. appl. Physiol. 63, 2396-2402.
15. Carolan, B. and Cafarelli, E. (1992) Adaptations in coactivation after isometric resistance training. J. appl. Physiol. 73, 911-917.
16. Carp, J. S. and Wolpaw, J. R. (1994) Motoneuron plasticity underlying operantly conditioned decrease in primate H-reflex. J. Neurophysiol. 72, 431-442.
17. Crenshaw, A. G., Karlsson, S., Styf, J., Bäcklund, T. and Fridén. J. (1995) Knee extension torque and intramuscular pressure of the vastus lateralis muscle during eccentric and concentric activities. Eur. J. Appl. Physiol. 70, 13-19.
18. Davies, C. T. M., Dooley, P., McDonagh, M. J. N. and White, M. J. (1985) Adaptation of mechanical properties of muscle to high force training in man. J. Physiol. (Lond.) 365, 277-284.
19. De Luca, C. J., LeFever, R. S., McCue, M. P., and Xenakis, A. P. (1982) Behavior of human motor units in different muscles during linearly varying contractions. J. Physiol. (Lond.) 329, 113-128.
20. Dowling, J. J., Konert, E., Ljucovic, P. and Andrews, D. M. (1994) Are humans able to voluntarily elicit maximum muscle force? Neurosci. Lett. 179, 25-28.
21. Duchateau, J. and Hainaut, K. (1984) Isometric or dynamic training: differential effects on mechanical properties of a human muscle. J. Appl. Physiol. 56, 296-301.
22. Duchateau, J. and Hainaut, K. (1987) Electrical and mechanical changes in immobilized human muscle. J. appl. Physiol. 62, 2168-2173.
23. Duchateau, J. and Hainaut, K. (1990) Effects of immobilization on contractile properties, recruitment and firing rates of human motor units. J. Physiol. (Lond.) 422, 55-65.
24. Dudley, G. A., Duvoisini, M. R., Adams, G. R., Meyer, R. A., Below, A. H. and Buchanan, P. (1992) Adaptations to unilateral lower limb suspension in humans. Aviat Space Environment. Med 63, 678-683.
25. Dudley, G. A., Tesch, P. A., Miller, B. J. and Buchanan, P. (1991) Importance of eccentric actions in performance adaptations to resistance training. Aviat. Space. Environ. Med. 62, 543-550.
26. Eloranta, V. and Komi, P. V. (1980) Function of the quadriceps femoris muscle under maximal concentric and eccentric contractions. Electromyogr. Clin, Neurophysiol. 20, 159-174.
27. Enoka, R. M. (1988) Muscle strength and its development: new perspectives. Sport Med. 6, 146-168.
28. Enoka, R. M. (1995) Morphological features and activation of motor units. J. Clin, Neurophysiol.
29. Enoka, R. M. (1996) Eccentric contractions require unique activation strategies by the nervous system. J. Appl. Physiol. 81, 2339-2346.
30. Enoka, R. M. and Behm, D. G. (1996) Strength training: foundation and strategies. In Textbook of Sports Medicine (Edited by Bergfeld, J. A. and Halpern, B.). Blackwell Science, Cambridge, MA.
31. Enoka, R. M. and Fuglevand, A. J. (1993) Neuromuscular basis of the maximum voluntary force capacity of muscle. In Current Issues in Biomechanics (Edited by Grabiner, M. D.), pp. 215-235. Human Kinetics, Champaign, IL.
32. Farmer, S. F., Swash, M., Ingram, D. A. and Stephens, J. A. (1993) Changes in motor unit synchronization following central nervous lesions in man. J. Physiol. (Lond.) 463, 83-105.
33. Faulkner, J. A. and Brooks, S. A. (1995) Muscle fatigue in old animals: unique aspects of fatigue in elderly human beings. In Fatigue: Neural and Muscular Mechanisms (Edited by Gandevia, S. C., Enoka, R. M., McComas, A. J., Stuart, D. G. and Thomas, C. K.), pp. 471-480. Plenum, New York.
34. Fisher, J. M., Meyer, R. A., Adams, G. R., Foley, J. M. and Potchen, J. E. (1990) Direct relationship between proton T2 and exercise intensity in skeletal muscle MR images. Invest, 25, 480-485.
35. 2 relaxation times and work during repetitive maximal voluntary exercise. J. appl. Physiol. 74, 2855-2859.
36. Freund, H. J., Büdingen, H. J. and Dietz, V. (1975) Activity of single motor units from human forearm muscles during voluntary isometric contractions. J. Neurophysiol. 38, 933-946.
37. Fuglevand, A. J., Bilodeau, M. and Enoka, R. M. (1995) Short-term immobilization has a minimal effect on the strength and fatigability of a human hand muscle. J. appl. Physiol. 78, 847-855.
38. Fuglsang-Frederiksen, A. and Scheel, U. (1978) Transient decrease in number of motor units after immobilisation in man. J. Neurol. Neurosurg. Psychiat. 41, 924-929.
39. Galganski, M. E., Fuglevand, A. J. and Enoka, R. M. (1993) Reduced control of motor output in a human hand muscle of elderly subjects during submaximal contractions. J. Neurophysiol. 69, 2108-2115.
40. Gandevia, S. C., Enoka, R. M., McComas, A. J., Stuart, D. G. and Thomas, C. K. (1995) Neural and Neuromuscular Aspects of Muscle Fatigue. Plenum, New York.
41. Gandevia, S. C. and Rothwell, J. C. (1987) Knowledge of motor commands and the recruitment of human motoneurons. Brain 110, 1117-1130.
42. Grabiner, M. D. and Enoka, R. M. (1995) Change in movement capabilities with aging. In Exercise and Sport Science Reviews, Vol. 23 (Edited by Holloszy, J. O.), pp. 65-104. Williams & Wilkins, Baltimore.
43. Grabiner, M. D., Owings, T. M., George, M. R. and Enoka, R. M. (1995) Eccentric contractions are specified a priori by the CNS, Proc. XV th Congr. Int. Soc. Biomech., Jyväskylä, Finland, 2-6 July.
44. Grimby, L. and Hannerz, J. (1977) Firing rate and recruitment order of toe extensor motor units in different modes of voluntary contraction. J. Physiol. (Lond.) 264, 865-879.
45. Häkkinen, K. and Komi, P. V. (1983) Electromyographic changes during strength training and detraining. Med. Sci. Sport. Exerc. 15, 455-460.
46. Hickson, R. C., Hidaka, K., Foster, C., Falduto, M. T. and Chatterton, R. T. (1994) Successive time courses of strength development and steriod hormone responses to heavy-resistance training. J. appl. Physiol. 76, 663-670.
47. Holstege, G. (1992) The emotional motor system. Eur J. Morphol. 30, 67-79.
48. Hortobágyi, T., Lambert, N. J. and Hill, J. P. (1997) Greater cross education following training with muscle lengthening than shortening. Med. Sci. Sports Exerc. 29, 107-112.
49. Hounsgaard, J., Hultborn, H., Jespersen, B. and Kiehn, O. (1984) Intrinsic membrane properties causing a bistable behavior of α-motoneurones, Exp. Brain Res. 55, 391-394.
50. Howard, J. D. and Enoka, R. M. (1991) Maximum bilateral contractions are modified by neurally mediated interlimb effects. J. appl. Physiol. 70, 306-316.
51. Howell, J. N., Fuglevand, A. J., Walsh, M. L. and Bigland-Ritchie, B. (1995) Motor unit activity during isometric and concentric-eccentric contractions of the human first dorsal interosseus muscles. J. Neurophysiol. 74, 901-904.
52. Jones, D. A. and Rutherford, O. M. (1987) Human muscle strength training: the effects of three different regimes and the nature of the resultant changes. J. Physiol. (Lond.) 391, 1-11.
53. Kadhiresan, V. A., Hassett, C. A. and Faulkner, J. A. (1996) Properties of single motor units in medical gastrocnemias. J. Physiol. (Lond.) 493, 543-552.
54. Kanda, K. and Hashizume, K. (1989) Changes in the properties of the medial gastrocnemius motor units in aging rats. J. Neurophysiol. 61, 737-746.
55. Keen, D. A., Yue, G. H. and Enoka, R. M. (1994) Training-related enhancement in the control of motor output in elderly humans. J. Appl. Physiol. 77, 2648-2658.
56. Kirkwood, P. A. and Sears, T. A. (1991) Cross-correlation analyses of motoneurone inputs in a coordinated motor act. In Springer Verlag Series in Synergetics: Neuronal Cooperativity (Edited by Kruger. J.), pp. 225-248. Springer, Berlin.
57. Kirkwood, P. A., Sears, T. A., Tuck, D. L. and Westgaard, R. H. (1982) Variations in the time course of the synchronization of intercostal motoneurones in cat. J. Physiol. (Lond). 327, 105-135.
58. Koh, T. J., Grabiner, M. D. and Clough, C. A. (1993) Bilateral deficit is larger for step than for ram isometric contractions. J. appl. Physiol. 74, 1200-1205
59. Komi, P. V. (1986) Training of muscle strength and power: interaction of neuromotoric. hypertrophic, and mechanical factors. Int. J. Sports Med. 7, 10-15.
60. Kukulka, C. G. and 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.
61. Kupfermann, I. (1991) Localization of higher cognitive and affective functions: the association cortices. In Principles of Neuroscience (3rd Edn) (Edited by Kandel, E. R., Schwartz, J. H. and Jessell, T. M.), pp. 824-838. Elsevier, New York.
62. Larsson, L. (1983) Histochemical characteristics of human skeletal muscle during aging. Acta Physiol. Scand. 117, 469-471.
63. Leong, B., Kamen, G., Patten, C. and Du, C. C. (1995) Motor unit discharge rates in older weight lifters during maximal voluntary contractions. Med. Sci. Sports Exerc. 27, S6.
64. Lømo, T. (1995) The modulation of muscle plasticity: the influence of electrical stimulation. Symp. 42nd Annual Meeting of the American College of Sport Medicine, Minneapolis, MN 31 May -3 June.
65. Macefield, V., Fuglevand, A. J. and Bigland-Ritchie, B. (1995) Force frequency relationships of motor units in extensor digitorum brevis. J. Physiol. (Lond.).
66. Marsden, C. D., Meadows, J. C. and Merton, P. A. (1983) 'Muscular wisdom' that minimizes fatigue during prolonged effort in man: peak rates of motoneuron discharge and slowing of discharge during fatigue. In Motor Control Mechanisms in Health and Disease (Edited by Desmedt, J. E.), pp. 169-211. Raven Press, New York.
67. McCartney, N., Moroz, D., Garner, S. H. and McComas, A. J. (1988) The effects of strength training in patients with selected neuromuscular disorder. Med. Sci. Sport Exerc. 20, 362-368.
68. Merton, P. A. (1954) Voluntary strength and fatigue. J. Physiol. (Lond.) 123, 553-546.
69. Milner-Brown, H. S., Stein, R. B. and Lee, R. G. (1975) Synchronization of human motor units: possible roles of exercise and supraspinal reflex. Electroenceph. Clin. Neurophysiol. 38, 245-254.
70. Monster, A. W. and Chan, H. (1977) Isometric force production by motor units of extensor digitorum communis muscle in man. J. Neurophysiol. 40, 1432-1443.
71. Moritani, T., Muramatsu, S. and Muro, M. (1988) Activity of motor units during concentric and eccentric contractions. Am J. Phys. Med. 66, 338-350.
72. Nakazawa, K., Kawakami, Y., Fukunaga, T., Yano, H. and Miyashita, M. (1993) Differences in activation patterns in elbow flexor muscles during isometric, concentric and eccentric contractions. Eur. J. Appl. Physiol. 66, 214-220.
73. Nardone, A., Romanò, C. and Schieppati, M. (1989) Selective recruitment of high-threshold human motor units during voluntary isotonic lengthening of active muscles. J. Physiol. (Lond.) 409, 451-471.
74. Nanci, M. V., Roi, G. S., Landoni, L., Minetti, A. E. and Cerretelli, P. (1989) Changes in forces, cross-sectional areas and neural activation during strength training and detraining of the human quadriceps. Eur. J. Appl. Physiol. 59, 310-319.
75. Newham, D. J., McCarthy, T. and Turner, J. (1991) Voluntary activation of human quadriceps during and after isokinetic exercise. J. appl. Physiol. 71, 2122-2126.
76. Nielsen, J., Crone, C. and Hultborn, H. (1993) H-reflexes are smaller in dances from The Royal Danish Ballet than in well-trained athletes. Eur. J. Appl. Physiol. 66, 116-121.
77. Nordstrom, M. A., Fuglevand, A. J. and Enoka, R. M. (1992) Estimating the strength of common input to human motoneurons from the cross-correlogram. J. Physiol. (Lond.) 453, 547-574.
78. Ohtsuki, T. (1983) Decrease in human voluntary isometric arm strength induced by simultaneous bilateral exertion. Behavior Brain Res. 7, 165-178.
79. Patten, C., Kamen, G., Rowland, D. and Du, C. C. (1995) Rapid adaptations of motor unit firing rate during the initial phase of strength development. Med. Sci. Sport Exerc. 27, S6.
80. Person, R. S. (1958) An electromyographic investigation on co-ordination of the activity of antagonist muscles in man during development of a motor habit. Pavlov J. Higher Nerrous Activity 8, 13-23.
81. Person, R. S. (1993) Spinal mechanisms of muscle contraction control. Sov. Sci. Rev. Sec. F. Phys. Gen. Biol. 6, 1-83.
82. Ploutz, L. L., Tesch, P. A., Biro, R. L. and Dudley, G. A. (1994) Effect of resistance training on muscle use during exercise. J. appl. Physol. 76, 1675-1681.
83. Poulin, M. J., Vandervoort, A. A., Paterson, D. H., Kramer, J. F. and Cunningham, D. A. (1992) Eccentric and concentric torques of knee and elbow extension in young and older men. Can. J. Sport Sci. 17, 3-7.
84. Rack, P. M. H. and 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.
85. Rogers, M. A. and Evans, W. J. (1993) Changes in skeletal muscle with aging: effects of exercise training. In Exercise and Sport Sciences Reviews, Vol. 21 (Edited by Holloszy, J. O.), pp. 65-102. Williams & Wilkins, Baltimore.
86. Rube, N. and Secher, N. H. (1990) Effect of training on central factors in fatigue following two- and one-leg static exercise in man. Acta Physiol. Scand. 141, 87-95.
87. Rutherford, O. M. and Jones, D. A. (1986) The role of learning and coordination in strength training. Eur. J. Appl. Physiol. 55, 100-105.
88. Sale, D. G. (1988) Neural adaptation to resistance training. Med. Sci. Sports Exerc. 20, S135-145.
89. Sale, D. G., McComas, A. J., MacDougall, J. D. and Upton, A. R. M. (1982) Neuromuscular adaptation in human thenar muscles following strength training and immobilization. J. Appl. Physiol. 53, 419-424.
90. Schantz, P. G., Moritani, T., Karlson, E., Johansson, E. and Lundh, A. (1989) Maximal voluntary force of bilateral and unilateral leg extension. Acta Physiol. Scand. 136, 185-192.
91. Schmied, A., Ivarsson, C. and Fetz, E. E. (1993) Short-term synchronization of motor units in human extensor digitorum communis muscle: relation to contractile properties and voluntary control. Exp. Brain Res. 97, 159-172.
92. Schmied, A., Vedel, J. P. and Pagni, S. (1994) Human spinal lateralization assessed from motoneurone synchronization: dependence on handedness and motor unit type. J. Physiol. (Lond.) 480, 369-387.
93. Schwindt, P. C. and Crill, W. E. (1980) Properties of a persistent inward current in normal and TEA-injected motoneurons. J. Neurophysiol. 43, 1700-1724.
94. Secher, N. H. (1975) Isometric rowing strength of experienced and inexperienced oarsmen. Med. Sci. Sport 1, 280-283.
95. Secher, N. H., Rorsgaard, S. and Secher, O. (1978) Contralateral influence on recruitment of curarized muscle fibres during maximal voluntary extension of the legs. Acta Physiol. Scand. 103, 456-462.
96. Secher, N. H., Rube, N. and Ellers, J. (1988) Strength of two- and one-leg extension in man. Acta Physiol. Scands. 134, 333-339.
97. Semmler, J. G. and Nordstrom, M. A. (1995) Influence of handedness on motor unit discharge properties and force tremor. Exp. Brain Res. 104, 115-125.
98. Spiegel, K., Stratton, J., Burke, J. R., Glendinning, D. S. and Enoka, R. M. (1996) Influence of age on the assessment of motor unit activation in a human hand muscle. Exp. Physiol. 81, 805-809.
99. Stålberg, E. and Fawcett, P. R. W. (1982) Macro EMG in healthy subjects of different ages. J. Neurol. Neurosurg. Psychiat. 45, 870-878.
100. Staron, R. S., Karapondo, D. L., Kraemer, W. J., Fry, A. C., Gordon, S. E., Falkel, J. E., Hagerman, F. C. and Hikida, R. S. (1994) Skeletal muscle adaptations during early phase of heavy-resistance training in men and women. J. appl. Physiol. 76, 1247-1255.
101. Tanji, J. and Kato, M. (1973) Firing rate of individual motor units in voluntary contraction of abductor digit minimi muscle in man. Exp. Neurol. 40, 771-783.
102. Tesch, P. A., Dudley, G. A. Duvoisin, M. R., Hather, B. M. and Harris, R. T. (1990) Force and EMG signal patterns during repeated bouts of concentric or eccentric muscle actions. Acta Physiol. Scand. 138, 263-271.
103. Thomas, C. K., Bigland-Ritchie, B. and Johansson, R. S. (1991) Force frequency relationships of human thenar motor units. J. Neurophysiol. 65, 1509-1516.
104. Vandervoort, A. A., Kramer, J. F. and Wharram, E. R. (1990) Eccentric knee strength of elderly females. J. Gerontol. Biol. Sci. 45, B125-128.
105. Vandervoort, A. A., Sale, D. G. and Moroz, J. (1984) Comparison of motor unit activation during unilateral and bilateral leg extension. J. appl. Physiol. 56, 46-51.
106. Westing, S. H., Cresswell, A. G. and Thorstensson, A. (1991) Muscle activation during maximal voluntary eccentric and concentric knee extension. Eur. J. Appl. Physiol. 62, 104-108.
107. Wilson, G. J., Young, W. B., Hurnall, G., Hood, K. P. and Steinebronn, M. (1994) The effect of slow versus fast rate of force development on resistance training induced changes in performance. J. Human Mvmt Stud. 27, 75-88.
108. Wolf, S. L., Segal, R. L. Heter, N. D. and Catlin, P. A. (1995) Contralateral and long latency effects of human biceps brachii stretch reflex conditioning. Exp. Brain Res. 107, 96-102.
109. Wolpaw, J. R. (1994) Acquisition and maintenance of the simplest motor skill: investigation of CNS mechanisms. Med. Sci. Sports Exerc. 26, 1475-1479.
110. Wolpaw, J. R. and Lee, C. L. (1989) Memory traces in primate spinal cord produced by operant conditioning of H-reflex. J. Neurophysiol. 61, 563-572.
111. Yue, G., Alexander, A. L., Laidlaw, D. H., Gmitro, A. F., Unger, E. C. and Enoka, R. M. (1994a) Sensitivity of muscle proton spin-spin relaxation time as an index of muscle activation. J. appl. Physiol. 77, 84-92.
112. Yue, G. H., Bilodeau, M. and Enoka, R. M. (1994b) Elbow-joint immobilization decreases fatigability and alters the pattern of activation in humans. Soc. Neurosci. Abstr. 20, 1205.
113. Yue, G. and Cole, K. J. (1992) Strength increases from the motor program: comparison of training with maximal voluntary and imagined muscle contractions. J. Neurophysiol. 67, 1114, 1123.
114. Yue, G., Fuglevand, A. J., Nordstrom, M. A. and Enoka, R. M. (1995a) Limitations of the surface-EMG technique for estimating motor unit synchronization. Biol. Cybernet. 73, 223-233.
115. Yue, G. H., Xue, M., Ng, T. and Enoka, R. M. (1995b) The decision to move may begin in the prefrontal cortex. Soc. Neurosci. Abstr. 21, 1421.
116. Young, W. B. and Bilby, G. E. (1993) The effect of voluntary effort to influence speed of contraction on strength, muscular power, and hypertrophy development. J. Strength Conditioning Res. 7, 172-178.