Sports Medicine

, Volume 36, Issue 11, pp 977–999 | Cite as

The Stretch-Shortening Cycle

A Model to Study Naturally Occurring Neuromuscular Fatigue
Review Article

Abstract

Neuromuscular fatigue has traditionally been examined using isolated forms of either isometric, concentric or eccentric actions. However, none of these actions are naturally occurring in human (or animal) ground locomotion. The basic muscle function is defined as the stretch-shortening cycle (SSC), where the preactivated muscle is first stretched (eccentric action) and then followed by the shortening (concentric) action. As the SSC taxes the skeletal muscles very strongly mechanically, its influence on the reflex activation becomes apparent and very different from the isolated forms of muscle actions mentioned above. The ground contact phases of running, jumping and hopping etc. are examples of the SSC for leg extensor muscles; similar phases can also be found for the upper-body activities. Consequently, it is normal and expected that the fatigue phenomena should be explored during SSC activities.

The fatigue responses of repeated SSC actions are very versatile and complex because the fatigue does not depend only on the metabolic loading, which is reportedly different among muscle actions. The complexity of SSC fatigue is well reflected by the recovery patterns of many neuromechanical parameters. The basic pattern of SSC fatigue response (e.g. when using the complete exhaustion model of hopping or jumping) is the bimodality showing an immediate reduction in performance during exercise, quick recovery within 1–2 hours, followed by a secondary reduction, which may often show the lowest values on the second day post-exercise when the symptoms of muscle soreness/damage are also greatest. The full recovery may take 4–8 days depending on the parameter and on the severity of exercise. Each subject may have their own time-dependent bimodality curve.

Based on the reviewed literature, it is recommended that the fatigue protocol is ‘completely’ exhaustive to reduce the important influence of inter-subject variability in the fatigue responses. The bimodality concept is especially apparent for stretch reflex responses, measured either in passive or active conditions. Interestingly, the reflex responses follow parallel changes with some of the pure mechanical parameters, such as yielding of the braking force during an initial ground contact of running or hopping. The mechanism of SSC fatigue and especially the bimodal response of performance deterioration and its recovery are often difficult to explain. The immediate post-exercise reduction in most of the measured parameters and their partial recovery 1–2 hours post-exercise can be explained primarily to be due to metabolic fatigue induced by exercise. The secondary reduction in these parameters takes place when the muscle soreness is highest.

The literature gives several suggestions including the possible structural damage of not only the extrafusal muscle fibres, but also the intrafusal ones. Temporary changes in structural proteins and muscle-tendon interaction may be related to the fatigue-induced force reduction. Neural adjustments in the supraspinal level could naturally be operative, although many studies quoted in this article emphasise more the influences of exhaustive SSC fatigue on the fusimotor-muscle spindle system. It is, however, still puzzling why the functional recovery lasts several days after the disappearance of muscle soreness. Unfortunately, this and many other possible mechanisms need more thorough testing in animal models provided that the SSC actions can be truly performed as they appear in normal human locomotion.

Keywords

Maximal Voluntary Contraction Muscle Spindle Eccentric Exercise Muscle Afferents Neuromuscular Fatigue 

Notes

Acknowledgements

Professor Komi was supported by grant 88/627/2005 from the Ministry of Education (Finland). The authors have no conflicts of interest that are directly relevant to the content of this review.

References

  1. 1.
    Gandevia SC. Spinal and supraspinal factors in human fatigue. Physiol Rev 2001; 81: 1725–89PubMedGoogle Scholar
  2. 2.
    Norman RW, Komi PV. Electromechanical delay in skeletal Norman RW, Komi PV. Electromechanical delay in skeletal Scand 1979; 106 (3): 241–8Google Scholar
  3. 3.
    Komi PV. Physiological and biomechanical correlates of muscle function: effects of muscle structure and stretch-shortening cycle on force and speed. Exerc Sport Sci Rev 1984; 12: 81–121PubMedGoogle Scholar
  4. 4.
    Komi PV. Stretch-shortening cycle: a powerful model to study normal and fatigue muscle. J Biomech 2000; 33: 1197–206PubMedGoogle Scholar
  5. 5.
    Komi PV, Norman RW. Preloading of the thrust phase in cross-country skiing. Int J Sports Med 1987; 8 Suppl. 1: 48–54PubMedGoogle Scholar
  6. 6.
    Davies CT, Thompson MW. Physiological responses to pro-longed exercise in ultramarathon athletes. J Appl Physiol 1986; 61 (2): 611–7PubMedGoogle Scholar
  7. 7.
    Millet GY, Lepers R, Maffiuletti NA, et al. Alterations of neuromuscular function after an ultramarathon. J Appl Physiol 2002; 92 (2): 486–92PubMedGoogle Scholar
  8. 8.
    Forsberg A, Tesch P, Karlsson J. Effect of prolonged exercise on muscle strength performance. In: Asmussenu E, Jorgensen K, editors. Biomechanics VI-A. Baltimore (MD): University Park Press, 1979: 62–7Google Scholar
  9. 9.
    Place N, Lepers R, Deley G, et al. Time course of neuromuscular alterations during a prolonged running exercise. Med Sci Sports Exerc 2004; 36 (8): 1347–56PubMedGoogle Scholar
  10. 10.
    Nicol C, Komi PV, Marconnet P. Fatigue effects of marathon running on neuromuscular performance II: changes in force, integrated electromyographic activity and endurance capacity. Scand J Med Sci Sports 1991; 1: 18–24Google Scholar
  11. 11.
    Millet GY, Martin V, Lattier G, et al. Mechanisms contributing to knee extensor strength loss after prolonged running exercise. J Appl Physiol 2003; 94 (1): 193–8PubMedGoogle Scholar
  12. 12.
    Gollhofer A, Komi PV, Fujitsuka N, et al. Fatigue during stretch-shortening cycle exercises II: changes in neuromuscu-lar activation patterns of human skeletal muscle. Int J Sports Med 1987; 8: 38–47PubMedGoogle Scholar
  13. 13.
    Gollhofer A, Komi PV, Miyashita M, et al. Fatigue during stretch-shortening cycle exercises: changes in mechanical performance of human skeletal muscle. Int J Sports Med 1987; 8 (2): 71–8PubMedGoogle Scholar
  14. 14.
    Lepers R, Pousson ML, Maffiuletti NA, et al. The effects of a prolonged running exercise on strength characteristics. Int J Sports Med 2000; 21 (4): 275–80PubMedGoogle Scholar
  15. 15.
    Strojnik V, Komi PV. Fatigue after submaximal intensive stretch-shortening cycle exercise. Med Sci Sports Exerc 2000; 32 (7): 1314–9PubMedGoogle Scholar
  16. 16.
    Martin V, Millet GY, Martin A, et al. Assessment of low-frequency fatigue with two methods of electrical stimulation. J Appl Physiol 2004; 97 (5): 1923–9PubMedGoogle Scholar
  17. 17.
    Davies CT, White MJ. Muscle weakness following dynamic exercise in humans. J Appl Physiol 1982; 53 (1): 236–41PubMedGoogle Scholar
  18. 18.
    Millet GY, Martin V, Maffiuletti NA, et al. Neuromuscular fatigue after a ski skating marathon. Can J Appl Physiol 2003; 28 (3): 434–45PubMedGoogle Scholar
  19. 19.
    Skurvydas A, Dudoniene V, Kalvenas A, et al. Skeletal muscle fatigue in long-distance runners, sprinters and untrained men after repeated drop jumps performed at maximal intensity. Scand J Med Sci Sports 2002 Feb; 12 (1): 34–9PubMedGoogle Scholar
  20. 20.
    Viitasalo JT, Komi PV, Jacobs I, et al. Effects of a prolonged cross-counting skiing on neuromuscular performance. In: Komi PV, editor. Exercise and sport biology. Champaign (IL): Human Kinetics, 1982; 12: 191–8Google Scholar
  21. 21.
    Pullinen T, Leynaert M, Komi PV. Neuromuscular function after marathon. Abstract book of the XIV ISB Congress; 1997 Aug 24–27; TokyoGoogle Scholar
  22. 22.
    Kuitunen S, Avela J, Kyröläinen H, et al. Acute and prolonged reduction in joint stiffness in humans after exhausting stretch-shortening cycle exercise. Eur J Appl Physiol 2002; 88: 107–16PubMedGoogle Scholar
  23. 23.
    Avela J, Kyröläinen H, Komi PV, et al. Reduced reflex sensitivity persists several days after long-lasting stretch-shortening cycle (SSC) exercise. J Appl Physiol 1999; 86 (4): 1292–300PubMedGoogle Scholar
  24. 24.
    Kuitunen S, Avela J, Kyrolainen H, et al. Voluntary activation and mechanical performance of human triceps surae muscle after exhaustive stretch-shortening cycle jumping exercise. Eur J Appl Physiol 2004; 91: 538–44PubMedGoogle Scholar
  25. 25.
    Ishikawa M, Dousset E, Avela J, et al. Changes in the soleus muscle architecture after exhausting stretch-shortening cycle exercise in humans. Eur J Appl Physiol 2006; 97: 298–306PubMedGoogle Scholar
  26. 26.
    Nicol C, Kuitunen S, Kyrolainen H, et al. Effects of long- and short-term fatiguing stretch-shortening cycle exercises on reflex EMG and force of the tendon-muscle complex. Eur J Appl Physiol 2003; 90: 470–9PubMedGoogle Scholar
  27. 27.
    Regueme SC, Barthèlemy J, Nicol C. Task- and time-dependent contralateral neural effects of a unilateral SSC fatiguing exercise [abstract]. 10th Annual Congress of the European College of Sport Science; 2005 Jul 13–16; BelgradeGoogle Scholar
  28. 28.
    Dousset E, Ishikawa M, Kyröläinen H, et al. Bimodal recovery from exhaustive stretch-shortening cycle exercise. Abstract book of the 8th Annual Congress of the European College of Sport Science; 2003 Jul 9–12; SalzburgGoogle Scholar
  29. 29.
    Skurvidas A, Jascaninas J, Zachovajevas P. Changes in height of jump, maximal voluntary contraction force and low-frequency fatigue after 100 intermittent or continuous jumps with maximal intensity. Acta Physiol Scand 2000; 169 (1): 55–62Google Scholar
  30. 30.
    Regueme SC, Nicol C, Barthelemy J, et al. Acute and delayed neuromuscular adjustments of the triceps surae muscle group to exhaustive stretch-shortening cycle fatigue. Eur J Appl Physiol 2005; 93 (4): 398–410PubMedGoogle Scholar
  31. 31.
    Martin V, Millet GY, Lattier G, et al. Effects of recovery modes after knee extensor muscles eccentric contractions. Med Sci Sports Exerc 2004; 36 (11): 1907–15PubMedGoogle Scholar
  32. 32.
    Cavagna GA, Saibene FP, Margaria R. Effect of negative work on the amount of positive work performed by an isolated muscle. J Appl Physiol 1965; 20: 157–8PubMedGoogle Scholar
  33. 33.
    Cavagna GA, Dusman B, Margaria R. Positive work done by a previously stretched muscle. J Appl Physiol 1968; 24: 21–32PubMedGoogle Scholar
  34. 34.
    Gregor RJ, Roy RR, Whiting WC, et al. Mechanical output of the cat soleus during treadmill locomotion: in vivo vs in situ characteristics. J Biomech 1988; 21 (9): 721–32PubMedGoogle Scholar
  35. 35.
    Komi PV. Elastic potentiation of muscles and its influence on sport performance. In: Baumann W, editor. Biomechanik und Sportliche Leistung. Schorndorf: Verlag Karl Hofmann, 1983: 59–70Google Scholar
  36. 36.
    Huijing PA. Elastic potential of muscle. In: Komi PV, editor. Strength and power in sport. Oxford: Blackwell Scientific Pulications, 1992: 151–68Google Scholar
  37. 37.
    van Ingen Schenau GJ, Bobbert MF, de Haan A. Does elastic energy enhance work and efficiency in the stretch-shortening cycle? J Appl Biomech 1997; 13: 389–415Google Scholar
  38. 38.
    Komi PV, Gollhofer A. Stretch reflex can have an important role in force enhancement during SSC-exercise. J Appl Bi-omech 1997; 33: 1197–206Google Scholar
  39. 39.
    Hoff AL, Geelen BA, Van den Berg JW. Calf muscle moment, work and efficiency in level walking; role of series elasticity. J Biomech 1983; 16 (7): 523–37Google Scholar
  40. 40.
    Belli A, Bosco C. Influence of stretch-shortening cycle on mechanical behaviour of triceps surae during hopping. Acta Physiol Scand 1992; 144 (4): 401–8PubMedGoogle Scholar
  41. 41.
    Griffiths RI. Shortening of muscle fibres during stretch of the active cat medial gastrocnemius muscle: the role of tendon compliance. J Physiol 1991; 436: 219–36PubMedGoogle Scholar
  42. 42.
    Ishikawa M, Komi PV. Effects of different dropping intensities on fascicle and tendinous tissue behaviour during stretch-shortening cycle exercise. J Appl Physiol 2004; 96: 848–52PubMedGoogle Scholar
  43. 43.
    Ishikawa M, Komi PV, Grey MJ, et al. Muscle-tendon interaction and elastic energy usage in human walking. J Appl Physiol 2005; 99 (2): 603–8PubMedGoogle Scholar
  44. 44.
    Komi PV, Nicol C. Stretch-shortening cycle fatigue: In: McIn-tosh B, Nigg B, Mester J, editors. Biomechanics and biology of movement. Champaign (IL): Human Kinetics Publishers, 2000: 385–408Google Scholar
  45. 45.
    Edwards RHT. Human muscle function and fatigue. Ciba Found Symp 1981; 82: 1–18PubMedGoogle Scholar
  46. 46.
    Booth FW, Thomason DB. Molecular and cellular adaptation of muscle in response to exercise: perspectives of various models. Physiol Rev 1991; 71 (2): 541–85PubMedGoogle Scholar
  47. 47.
    Asmussen E. Muscle fatigue. Med Sci Sports 1979; 11 (4): 313–21PubMedGoogle Scholar
  48. 48.
    Hortobagyi T, Lambert NL, Kroll WP. Voluntary and reflex responses to fatigue with stretch-shortening cycle exercise. Can J Sports Science 1991; 6: 142–50Google Scholar
  49. 49.
    Horita T, Komi PV, Nicol C, et al. Interaction between prelanding activities and stiffness regulation of the knee joint musculoskeletal in the drop jump: implications to performance. Eur J Appl Physiol 2002; 88 (1-2): 76–84PubMedGoogle Scholar
  50. 50.
    Strojnik V, Nicol C, Komi PV. Fatigue during one-week tourist alpine skiing. In: Müller E, Schwameder H, Raschner C, et al., editors. Science and skiing II. Hamburg: Kovač, 2001: 599–607Google Scholar
  51. 51.
    Horita T, Komi PV, Nicol N, et al. Stretch shortening cycle fatigue: interactions among joint stiffness, reflex, and muscle mechanical performance in the drop jump. Eur J Appl Physiol 1996; 73 (5): 393–403Google Scholar
  52. 52.
    Nicol C, Komi PV, Horita T, et al. Reduced stretch-reflex sensitivity after exhaustive stretch-shortening cycle exercise. Eur J Appl Physiol 1996; 72 (5-6): 401–9Google Scholar
  53. 53.
    Avela J, Komi PV. Reduced stretch reflex sensitivity and muscle stiffness after long-lasting stretch-shortening muscle cycle (SSC) exercise. Eur J Appl Physiol 1998; 78 (5): 403–10Google Scholar
  54. 54.
    Horita T. Stiffness regulation during stretch-shortening cycle exercise [dissertation]. Jyväskylä: University of Jyväskylä, Department of Biology of Physical Activity, 2000Google Scholar
  55. 55.
    Nicol C, Komi PV, Marconnet P. Fatigue effects of marathon-running on neuromuscular performance I: changes in muscle force and stiffness characteristics. Scand J Med Sci Sports 1991; 1: 10–7Google Scholar
  56. 56.
    Horita T, Komi PV, Hamalainen I, et al. Exhausting stretch-shortening cycle (SSC) exercise causes greater impairment in SSC performance than in pure concentric performance. Eur J Appl Physiol 2003; 88: 527–34PubMedGoogle Scholar
  57. 57.
    Horita T, Komi PV, Nicol C, et al. Effect of exhausting stretch-shortening cycle exercise on the time course of mechanical behaviour in the drop jump: possible role of muscle damage. Eur J Appl Physiol 1999; 79: 160–7Google Scholar
  58. 58.
    Komi PV, Gollhofer A, Schmidtbleicher D, et al. Interaction between man and shoe in running: considerations for more comprehensive measurement approach. Int J Sports Med 1987; 8 (3): 196–202PubMedGoogle Scholar
  59. 59.
    Kyröläinen H, Pullinen T, Candau R, et al. Effects of marathon running on running economy and kinematics. Eur J Appl Physiol 2001; 82 (4): 297–304Google Scholar
  60. 60.
    Finni T, Kyröläinen H, Avela J, et al. Maximal but not submaximal performance is reduced by constant-speed 10-km run. J Sports Med Phys Fitness 2003; 43 (4): 411–7PubMedGoogle Scholar
  61. 61.
    Nicol C, Komi PV, Marconnet P. Effects of marathon fatigue on running kinematics and economy. Scand J Med Sci Sports 1991; 1: 195–204Google Scholar
  62. 62.
    Johansson H, Sojka P. Pathophysiological mechanisms involved in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes: a hypothesis. Med Hypotheses 1991; 35: 196–203PubMedGoogle Scholar
  63. 63.
    Radhakrishnan R, Moore SA, Sluka KA. Unilateral carrageenan injection into muscle or joint induces chronic bilateral hyperalgesia in rats. Pain 2003; 104: 567–77PubMedGoogle Scholar
  64. 64.
    Woolf CJ. Long term alterations in the excitability of the flexion reflex produced by peripheral tissue injury in the chronic decerebrate rat. Pain 1984; 18: 325–43PubMedGoogle Scholar
  65. 65.
    Zijdewind I, Zwarts MJ, Kernell D. Influence of a voluntary fatigue test on the contralateral homologous muscle in humans? Neurosci Lett 1998; 253: 41–4PubMedGoogle Scholar
  66. 66.
    Todd G, Petersen NT, Taylor JL, et al. The effect of a contralateral contraction on maximal voluntary activation and central fatigue in elbow flexor muscles. Exp Brain Res 2003; 150 (3): 308–13PubMedGoogle Scholar
  67. 67.
    Rattey J, Martin PG, Kay D, et al. Contralateral muscle fatigue in human quadriceps muscle: evidence for a centrally mediated fatigue response and cross-over effect. Pflugers Arch 2005; 20: 1–9Google Scholar
  68. 68.
    Zijdewind I, Kernell D. Bilateral interactions during contractions of intrinsic hand muscles. J Neurophysiol 2001; 85: 1907–13PubMedGoogle Scholar
  69. 69.
    Fukunaga T, Kubo K, Kawakami Y, et al. In vivo behaviour of human muscle tendon during walking. Proc Biol Sci 2001 Feb 7; 268 (1464): 229–33PubMedGoogle Scholar
  70. 70.
    Roberts TJ, Marsh RL, Weyand PG, et al. Muscular force in running turkeys: the economy of minimizing work. Science 1997; 275 (5303): 1113–5PubMedGoogle Scholar
  71. 71.
    Ishikawa M, Niemela E, Komi PV. Interaction between fascicle and tendinous tissues in short contact stretch-shortening cycle exercise with varying eccentric intensities. J Appl Physiol 2005; 99 (1): 217–23PubMedGoogle Scholar
  72. 72.
    Hough T. Ergographic studies in muscle soreness. Am J Appl Physiol 1902; 7: 76–92Google Scholar
  73. 73.
    Asmussen E. Observations on experimental muscle soreness. Acta Rheumatol Scand 1956; 2: 109–16PubMedGoogle Scholar
  74. 74.
    Lieber R, Shah S, Fridén J. Cytoskeletal disruption after eccentric contraction-induced muscle injury. Clin Orthop Relat Res 2002; 403 Suppl.: S90–9PubMedGoogle Scholar
  75. 75.
    Clarkson PM, Newham DJ. Associations between muscle soreness, damage, and fatigue. In: Gandevia SC, Enoka RM, McComas AJ, et al., editors. Fatigue. New-York: Plenum Press, 1995: 457–76Google Scholar
  76. 76.
    Fridén J, Lieber RL. Eccentric exercise-induced injuries to contractile and cytoskeletal muscle fibre components. Acta Physiol Scand 2001; 171: 321–6PubMedGoogle Scholar
  77. 77.
    Komi PV, Rusko H. Quantitative evaluation of mechanical and electrical changes during fatigue loading of eccentric and concentric work. Scand J Rehabil Med Suppl 1974; 3: 121–6PubMedGoogle Scholar
  78. 78.
    Whitehead NP, Weerakkody NS, Gregory JE, et al. Changes in passive tension of muscle in humans and animals after eccentric exercise. J Physiol 2001; 533 (Pt 2): 593–604PubMedGoogle Scholar
  79. 79.
    Jones C, Allen T, Talbot J, et al. Changes in the mechanical properties of human and amphibian muscle after eccentric exercise. Eur J Appl Physiol 1997; 76 (1): 21–31Google Scholar
  80. 80.
    Fridén J, Sjöström M, Ekblom B. Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 1983; 4: 170–6PubMedGoogle Scholar
  81. 81.
    Newham DJ, McPhail G, Mills KR, et al. Ultrastructural changes after concentric and eccentric contractions of human muscle. J Neurol Sci 1983; 61: 109–22PubMedGoogle Scholar
  82. 82.
    Armstrong RB. Initial events in exercise-induced muscular injury. Med Sci Sports Exerc 1990; 22 (4): 429–35PubMedGoogle Scholar
  83. 83.
    Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle fibre injury. Sports Med 1991; 12: 184–207PubMedGoogle Scholar
  84. 84.
    Féasson L, Stockholm D, Freyssenet D, et al. Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J Physiol 2002; 543 (Pt 1): 297–306PubMedGoogle Scholar
  85. 85.
    Yu JG, Furst DO, Thornell LE. The mode of myofibril remodelling in human skeletal muscle affected by DOMS induced by eccentric contractions. Histochem Cell Biol 2003; 119 (5): 383–93PubMedGoogle Scholar
  86. 86.
    Yu JG, Carlsson L, Thornell LE. Evidence for myofibril remodeling as opposed to myofibril damage in human muscles with DOMS: an ultrastructural and immunoelectron microscopic study. Histochem Cell Biol 2004; 121 (3): 219–27PubMedGoogle Scholar
  87. 87.
    Fowles JR, Sale DG, MacDougall JD. Reduced strength after passive stretch of the human plantarflexors. J Appl Physiol 2000; 89: 1179–88PubMedGoogle Scholar
  88. 88.
    Avela J, Kyröläinen H, Komi PV. Neuromuscular changes after long-lasting mechanically and electrically elicited fatigue. Eur J Appl Physiol 2001; 85 (3-4): 317–25PubMedGoogle Scholar
  89. 89.
    Taylor DC, Dalton JD, Seaber AV, et al. Viscoelastic properties of muscle-tendon units: the biomechanical effects of stretching. Am J Sports Med 1990; 18: 300–9PubMedGoogle Scholar
  90. 90.
    Taylor DC, Brooks DE, Ryan JB. Viscoelastic characteristics of muscle: passive stretching versus muscular contractions. Med Sci Sports Exerc 1997; 29 (12): 1619–24PubMedGoogle Scholar
  91. 91.
    Magnusson SP, Simonsen EB, Aagaard P, et al. Contraction-specific changes in passive torque in human skeletal muscle. Acta Physiol Scand 1995; 155: 377–86PubMedGoogle Scholar
  92. 92.
    Purslow PP. Strain-induced reorientation of an intramuscular connective tissue network: implication for passive muscle elasticity. J Biomech 1989; 22: 21–31PubMedGoogle Scholar
  93. 93.
    Lieber RL, Woodburn TM, Friden J. Muscle damage induced by eccentric contractions of 25% strain. J Appl Physiol 1991; 70: 2498–507PubMedGoogle Scholar
  94. 94.
    Avela J, Finni T, Liikavainio T. Neural and mechanical re-sponses of the triceps surae muscle group after 1h of repeated fast passive stretches. J Appl Physiol 2004; 96 (6): 2325–32PubMedGoogle Scholar
  95. 95.
    Nicol C, Komi PV. Significance of passively induced stretch reflexes on Achilles tendon force enhancement. Muscle Nerve 1998; 21: 1546–8PubMedGoogle Scholar
  96. 96.
    Gregory JE, Morgan DL, Proske U. Responses of muscle spindles following a series of eccentric contractions. Exp Brain Res 2004; 157 (2): 234–40PubMedGoogle Scholar
  97. 97.
    Trappe TA, Carrithers JA, White F, et al. Titin and nebulin content in human skeletal muscle following eccentric resistance exercise. Muscle Nerve 2002; 25 (2): 289–92PubMedGoogle Scholar
  98. 98.
    Bigland-Ritchie B. EMG/force relations and fatigue of human voluntary contractions. Exerc Sport Sci Rev 1981; 9: 451–9Google Scholar
  99. 99.
    LöNoscher G, Cresswell AG, Thorstensson A. Excitatory drive to the α-motoneuron pool during fatiguing submaximal contraction in man. J Physiol 1996; 491: 271–80Google Scholar
  100. 100.
    Bigland-Ritchie B, Johansson R, Lippold OCJ, et al. Contractile speed and EMG changes during fatigue of sustained maximal voluntary contraction. J Neurophysiol 1983; 50: 313–24PubMedGoogle Scholar
  101. 101.
    Gandevia SC, Allen GM, McKenzie DK. Central fatigue: critical issues, quantification and practical implications. Adv Exp Med Biol 1995; 384: 281–94PubMedGoogle Scholar
  102. 102.
    Merton PA. Voluntary strength and fatigu. J Physiol 1954; 123: 553–6PubMedGoogle Scholar
  103. 103.
    Brasil-Neto JP, Pascual-Leone A, Valls-sole J, et al. Postexercise depression of motor evoked potentials: a measure of central nervous system fatigue. Exp Brain Res 1993; 74: 649–52Google Scholar
  104. 104.
    Brasil-Neto JP, Cohen LG, Hallett M. Central fatigue as revealed by postexercise decrement of motor evoked potential. Muscle Nerve 1994; 17: 713–9PubMedGoogle Scholar
  105. 105.
    LöNoscher WN, Nordlund MM. Central fatigue and motor cortical excitability during repeated shortening and lengthening actions. Muscle Nerve 2002; 25 (6): 864–72Google Scholar
  106. 106.
    Kalmar JM, Cafarelli E. Caffeine: a valuable tool to study central fatigue in humans? Exerc Sport Sci Rev 2004; 32 (4): 143–7PubMedGoogle Scholar
  107. 107.
    Millet GY, Lepers R. Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med 2004; 34 (2): 105–16PubMedGoogle Scholar
  108. 108.
    Qerama E, Fuglsang-Frederiksen A, Kasch H, et al. Effects of evoked pain on the electromyogram and compound muscle action potential of the brachial biceps muscle. Muscle Nerve 2005; 31 (1): 25–33PubMedGoogle Scholar
  109. 109.
    Le Pera D, Graven-Nielsen T, Valeriani M, et al. Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clin Neurophysiol 2001; 112 (9): 1633–41PubMedGoogle Scholar
  110. 110.
    Nicol C, Komi PV, Avela J. Stretch-shortening cycle fatigue reduces stretch-reflex response. In: Abstract book of the 1996 International Pre-Olympic Scientific Congress; 1996 Jul 10–14; Dallas (TX), 108Google Scholar
  111. 111.
    Svensson P, De Laat A, Graven-Nielsen T, et al. Experimental jaw-muscle pain does not change heteronymous H-reflexes in the human temporal muscle. Exp Brain Res 1998; 121: 311–8PubMedGoogle Scholar
  112. 112.
    Matre DA, Sinkjaer T, Svensson P, et al. Experimental muscle pain increases the human stretch reflex. Pain 1998; 75: 331–9PubMedGoogle Scholar
  113. 113.
    Burke D, Hagbarth KE, Skuse NF. Voluntary activation of spindle endings in human muscles temporarily paralysed by nerve pressure. J Physiol 1979; 287: 329–36PubMedGoogle Scholar
  114. 114.
    Macefield G, Hagbarth K-E, Gorman R, et al. Decline in spindle support to α-motoneurones during sustained voluntary contractions. J Physiol 1991; 440: 497–512PubMedGoogle Scholar
  115. 115.
    Hagbarth K-E, Kunesch EJ, Nordin M, et al. Gamma loop contribution to maximal voluntary contractions in man. J Physiol 1986; 380: 575–91PubMedGoogle Scholar
  116. 116.
    Bongiovanni LG, Hagbarth K-E. Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man. J Physiol 1990; 423: 1–14PubMedGoogle Scholar
  117. 117.
    Emonet-Denand F, Laporte Y. Selective neuromuscular block in extrafusal junctions of skeleton-fusimotor axons produced by high frequency repetitive stimulation. C R Hebd Seances Acad Sci D Sci Nat 1974; 279: 2083–5Google Scholar
  118. 118.
    Avela J, Finni T, Liikavainio T, et al. Neural and mechanical responses of the triceps surae muscle group after 1 hour of repeated fast stretches (highlighted topic/neural control of movement). J Appl Physiol 2004; 96: 2325–33PubMedGoogle Scholar
  119. 119.
    Decorte L, Emonet-Denand F, Harker DW, et al. Glycogen depletion elicited in tenuissimus intrafusal muscle fibres by stimulation of static gamma-axons in the cat. J Physiol 1984; 346: 341–52PubMedGoogle Scholar
  120. 120.
    Yoshimura A, Shimomura Y, Murakami T, et al. Glycogen depletion of the intrafusal fibers in a mouse muscle spindle during prolonged swimming. Am J Physiol 1996; 271 (2 Pt 2): R398–R408PubMedGoogle Scholar
  121. 121.
    Fukami Y. The effects of NH3 and CO2 on the sensory ending of mammalian muscle spindles: intracellular pH as a possible mechanism. Brain Res 1988; 463: 140–3PubMedGoogle Scholar
  122. 122.
    Asmussen E, Mazin BA. Central nervous component in local muscular fatigue. Eur J Appl Physiol 1978; 38: 9–15Google Scholar
  123. 123.
    Bigland-Ritchie BR, Dawson NJ, Johansson R, et al. Reflex origin for the slowing of motoneurone firing rates in fatiguing human voluntary contractions. J Physiol 1986; 379: 451–9PubMedGoogle Scholar
  124. 124.
    LöNoscher WN, Cresswell AG, Thorstensson A. Central Fatigue during a long-lasting submaximal contraction of the triceps surae. Exp Brain Res 1996; 108 (2): 305–14Google Scholar
  125. 125.
    Kniffki KD, Mense S, Schmidt RF. Responses of group IV afferent units from skeletal muscle to stretch, contraction and chemical stimulation. Exp Brain Res 1978; 31: 511–22PubMedGoogle Scholar
  126. 126.
    Rotto DM, Kaufman MP. Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J Appl Physiol 1988; 64: 2306–13PubMedGoogle Scholar
  127. 127.
    Decherchi P, Darques JL, Jammes Y. Modifications of afferent activities from tibialis anterior muscle in rat by tendon vibrations, increase of interstitial potassium and lactate concentra-tion and electrically-induced fatigue. J Peripher Nerv Syst 1998; 3 (4): 1–10Google Scholar
  128. 128.
    Mense S, Meyer H. Bradykinin-induced modulation of the response behaviour of different types of feline group III and IV muscle receptors. J Physiol 1988; 398: 49–63PubMedGoogle Scholar
  129. 129.
    Fields HL. Pain. New York: McGraw-Hill, 1987: 35Google Scholar
  130. 130.
    Travell J, Rinzler S, Herman M. Pain and disability of the shoulder and arm: treatment by intramuscular infiltration with procaine hydrochloride. JAMA 1942; 120: 417–22Google Scholar
  131. 131.
    Ljubisavljevic M, Anastasijevic R, Trifunjagic D. Changes in fusimotor discharge rate provoked by isotonic fatiguing muscle contractions in decerebrate cats. Brain Res 1995; 673 (1): 126–32PubMedGoogle Scholar
  132. 132.
    Jovanovićc K, Anastasijevićc R, Vućco J. Reflex effects on gamma fusimotor neurones of chemically induced discharges in small-diameter muscle afferents in decerebrate cats. Brain Res 1990; 521: 89–94Google Scholar
  133. 133.
    Ljubisavljevic M, Anastasijevic R. Fusimotor-induced changes in muscle spindle outflow and responsiveness in muscle fatigue in decerebrate cats. Neuroscience 1994; 63 (1): 339–48PubMedGoogle Scholar
  134. 134.
    Djupsjöbacka M, Johansson H, Bergenheim M, et al. Influence on the γ-muscle spindle system from muscle afferents stimulated by increased intramuscular concentrations of bradykinin and 5-HT. Neurosci Res 1995; 22: 325–33PubMedGoogle Scholar
  135. 135.
    Matre DA, Sinkjaer T, Knardahl S, et al. The influence of experimental muscle pain on the human soleus stretch reflex during sitting and walking. Clin Neurophysiol 1999; 110 (12): 2033–43PubMedGoogle Scholar
  136. 136.
    Cleland C, Rymer W, Edwards F. Force-sensitive interneurons in the spinal cord of the cat. Science 1982; 217: 652–5PubMedGoogle Scholar
  137. 137.
    Duchateau J, Hainaut K. Behaviour of short and long latency reflexes in fatigued human muscles. J Physiol 1993; 471: 787–99PubMedGoogle Scholar
  138. 138.
    Garland J, McComas AJ. Reflex inhibition of human soleus muscle during fatigue. J Physiol 1990; 429: 17–27PubMedGoogle Scholar
  139. 139.
    Garland J. Role of small diameter afferents in reflex inhibition during human muscle fatigue. J Physiol 1991; 435: 547–58PubMedGoogle Scholar
  140. 140.
    Brunetti O, Della Torre G, Lucchi ML, et al. Inhibition of muscle spindle afferent activity during masseter muscle fatigue in the rat. Exp Brain Res 2003; 52 (2): 251–62Google Scholar

Copyright information

© Adis Data Information BV 2006

Authors and Affiliations

  1. 1.Department of Physiology of Physical Activity, UPRES-EA 3285University of the MediterraneanMarseillesFrance
  2. 2.Neuromuscular Research Center, Department of Biology of Physical ActivityUniversity of JyväskyläJyväskyläFinland

Personalised recommendations