Locomotor muscle fatigue is not critically regulated after prior upper body exercise

Journal of Applied Physiology

Volumn 119, Issue 7, 2015, Pages 840-850

  Johnson, M A ^a   Sharpe, G R ^a   Williams, N C ^a   Hannah, R ^b  

^a NOTTINGHAM TRENT UNIVERSITY   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Central fatigue; Exercise tolerance; Perceived exertion; Peripheral fatigue

Indexed keywords

ADULT; ARM; DYNAMOMETER; ELECTROMYOGRAPHY; ELECTROSTIMULATION; EXERCISE; EXERCISE TOLERANCE; FEMORAL NERVE; HEART RATE; HUMAN; LEG; LOCOMOTION; MALE; MUSCLE CONTRACTION; MUSCLE FATIGUE; PHYSIOLOGY; SKELETAL MUSCLE; YOUNG ADULT;

ADULT; ARM; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; EXERCISE; EXERCISE TOLERANCE; FEMORAL NERVE; HEART RATE; HUMANS; LEG; LOCOMOTION; MALE; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE STRENGTH DYNAMOMETER; MUSCLE, SKELETAL; YOUNG ADULT;

EID: 84943761209     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00072.2015     Document Type: Article

References (80)

1. Adreani CM, Hill JM, Kaufman MP. Responses of group III and IV muscle afferents to dynamic exercise. J Appl Physiol 82: 1811-1817, 1997.
2. Altman DG, Gardner MJ. Means and their differences. In: Statistics with Confidence, edited by Altman DG, Machin D, Bryant TN, and Gardner MJ. London: BMJ, 2000, p. 28-35.
3. Amann M. Central and peripheral fatigue: interaction during cycling exercise in humans. Med Sci Sports Exerc 43: 2039-2045, 2011.
4. Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Implications of group III and IV muscle afferents for highintensity endurance exercise performance in humans. J Physiol 589: 5299-5309, 2011.
5. Amann M, Dempsey JA. Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol 586: 161-173, 2008.
6. Amann M, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 587: 271-283, 2009.
7. Amann M, Romer LM, Pegelow DF, Jacques AJ, Hess CJ, Dempsey JA. Effects of arterial oxygen content on peripheral locomotor muscle fatigue. J Appl Physiol 101: 119-127, 2006.
8. Amann M, Romer LM, Subudhi AW, Pegelow DF, Dempsey JA. Severity of arterial hypoxaemia affects the relative contributions of peripheral muscle fatigue to exercise performance in healthy humans. J Physiol 581: 389-403, 2007.
9. Amann M, Secher NH. Point: Afferent feedback from fatigued locomotor muscles is an important determinant of endurance exercise performance. J Appl Physiol 108: 452-454, 2010.
10. Amann M, Venturelli M, Ives SJ, McDaniel J, Layec G, Rossman MJ, Richardson RS. Peripheral fatigue limits endurance exercise via a sensory feedback-mediated reduction in spinal motoneuronal output. J Appl Physiol 115: 355-364, 2013.
11. + uptake in inactive muscles during intense exercise in man. J Physiol 488: 219-229, 1995.
12. Bangsbo J, Madsen K, Kiens B, Richter EA. Effect of muscle acidity on muscle metabolism and fatigue during intense exercise in man. J Physiol 495: 587-596, 1996.
13. Barry BK, Enoka RM. The neurobiology of muscle fatigue: 15 years later. Integr Comp Biol 47: 465-473, 2007.
14. Bigland-Ritchie BR, Dawson NJ, Johansson RS, Lippold OC. Reflex origin for the slowing of motoneurone firing rates in fatigue of human voluntary contractions. J Physiol 379: 451-459, 1986.
15. Blanchfield AW, Hardy J, De Morree HM, Staiano W, Marcora SM. Talking yourself out of exhaustion: the effects of self-talk on endurance performance. Med Sci Sports Exerc 46: 998-1007, 2014.
16. Bland JM, Altman DG. Measurement error. BMJ 313: 744, 1996.
17. Bogdanis GC, Nevill ME, Lakomy HK. Effects of previous dynamic arm exercise on power output during repeated maximal sprint cycling. J Sports Sci 12: 363-370, 1994.
18. Borg G. Borg's Perceived Exertion and Pain Scales. Champaign, IL: Human Kinetics, 1998.
19. Buckthorpe MW, Hannah R, Pain TG, Folland JP. Reliability of neuromuscular measurements during explosive isometric contractions, with special reference to electromyography normalization techniques. Muscle Nerve 46: 566-576, 2012.
20. Burnley M, Vanhatalo A, Fulford J, Jones AM. Similar metabolic perturbations during all-out and constant force exhaustive exercise in humans: a (31)P magnetic resonance spectroscopy study. Exp Physiol 95: 798-807, 2010.
21. Cairns SP, Lindinger MI. Do multiple ionic interactions contribute to skeletal muscle fatigue? J Physiol 586: 4039-4054, 2008.
22. Chapman AR, Vicenzino B, Blanch P, Hodges PW. Patterns of leg muscle recruitment vary between novice and highly trained cyclists. J Electromyogr Kinesiol 18: 359-371, 2008.
23. Chapman AR, Vicenzino B, Blanch P, Knox JJ, Hodges PW. Leg muscle recruitment in highly trained cyclists. J Sports Sci 24: 115-124, 2006.
24. Crewe H, Tucker R, Noakes TD. The rate of increase in rating of perceived exertion predicts the duration of exercise to fatigue at a fixed power output in different environmental conditions. Eur J Appl Physiol 103: 569-577, 2008.
25. Darques JL, Decherchi P, Jammes Y. Mechanisms of fatigue-induced activation of group IV muscle afferents: the roles played by lactic acid and inflammatory mediators. Neurosci Lett 257: 109-112, 1998.
26. De Luca CJ. The use of electromyography in biomechanics. J Appl Biomech 13: 135-163, 1997.
27. De Luca CJ, Gilmore LD, Kuznetsov M, Roy SH. Filtering the surface EMG signal: movement artifact and baseline noise contamination. J Biomech 43: 1573-1579, 2010.
28. de Ruiter CJ, Hoddenbach JG, Huurnink A, de Haan A. Relative torque contribution of vastus medialis muscle at different knee angles. Acta Physiol (Oxf) 194: 223-237, 2008.
29. de Ruiter CJ, Kooistra RD, Paalman MI, de Haan A. Initial phase of maximal voluntary and electrically stimulated knee extension torque development at different knee angles. J Appl Physiol 97: 1693-1701, 2004.
30. Decorte N, Lafaix PA, Millet GY, Wuyam B, Verges S. Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scand J Med Sci Sports 22: 381-391, 2012.
31. Dempsey JA. New perspectives concerning feedback influences on cardiorespiratory control during rhythmic exercise and on exercise performance. J Physiol 590: 4129-4144, 2012.
32. Eston R, Faulkner J, St. Clair Gibson A, Noakes T, Parfitt G. The effect of antecedent fatiguing activity on the relationship between perceived exertion and physiological activity during a constant load exercise task. Psychophysiology 44: 779-786, 2007.
33. Fitts RH. The cross-bridge cycle and skeletal muscle fatigue. J Appl Physiol 104: 551-558, 2008.
34. Gagnon P, Saey D, Vivodtzev I, Laviolette L, Mainguy V, Milot J, Provencher S, Maltais F. Impact of preinduced quadriceps fatigue on exercise response in chronic obstructive pulmonary disease and healthy subjects. J Appl Physiol 107: 832-840, 2009.
35. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81: 1725-1789, 2001.
36. Grant MC, Robergs R, Baird MF, Baker JS. The effect of prior upper body exercise on subsequent wingate performance. Biomed Res Int 2014: 329328, 2014.
37. Grippo A, Carrai R, Chiti L, Bruni GI, Scano G, Duranti R. Effect of limb muscle fatigue on perception of respiratory effort in healthy subjects. J Appl Physiol 109: 367-376, 2010.
38. Hannah R, Minshull C, Buckthorpe MW, Folland JP. Explosive neuromuscular performance of males versus females. Exp Physiol 97: 618-629, 2012.
39. Hannah R, Minshull C, Folland JP. Whole-body vibration does not influence knee joint neuromuscular function or proprioception. Scand J Med Sci Sports 23: 96-104, 2013.
40. Hannah R, Minshull C, Smith SL, Folland JP. Longer electromechanical delay impairs hamstrings explosive force versus quadriceps. Med Sci Sports Exerc 46: 963-972, 2014.
41. Hannah R, Stannard RL, Minshull C, Artioli GG, Harris RC, Sale C. β-Alanine supplementation enhances human skeletal muscle relaxation speed but not force production capacity. J Appl Physiol 118: 604-612, 2015.
42. Hodges PW, Bui BH. A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. Electroencephalogr Clin Neurophysiol 101: 511-519, 1996.
43. Hopkins WG. Measures of reliability in sports medicine and science. Sports Med 30: 1-15, 2000.
44. Jacobs I, Hermiston AJ, Symons JD. Effects of prior exercise or ammonium chloride ingestion on muscular strength and endurance. Med Sci Sports Exerc 25: 809-814, 1993.
45. Jammes Y, Balzamo E. Changes in afferent and efferent phrenic activities with electrically induced diaphragmatic fatigue. J Appl Physiol 73: 894-902, 1992.
46. Johnson MA, Mills DE, Brown PI, Sharpe GR. Prior upper body exercise reduces cycling work capacity but not critical power. Med Sci Sports Exerc 46: 802-808, 2014.
47. Karlsson J, Bonde-Petersen F, Henriksson J, Knuttgen HG. Effects of previous exercise with arms or legs on metabolism and performance in exhaustive exercise. J Appl Physiol 38: 763-767, 1975.
48. Kooistra RD, de Ruiter CJ, de Haan A. Conventionally assessed voluntary activation does not represent relative voluntary torque production. Eur J Appl Physiol 100: 309-320, 2007.
49. Kufel TJ, Pineda LA, Mador MJ. Comparison of potentiated and unpotentiated twitches as an index of muscle fatigue. Muscle Nerve 25: 438-444, 2002.
50. Laviolette L, Laveneziana P, ERS Research Seminar Faculty. Dyspnoea: a multidimensional and multidisciplinary approach. Eur Respir J 43: 1750-1762, 2014.
51. Light AR, Hughen RW, Zhang J, Rainier J, Liu Z, Lee J. Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TRPV1. J Neurophysiol 100: 1184-1201, 2008.
52. Mador MJ, Kufel TJ, Pineda L. Quadriceps fatigue after cycle exercise in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 161: 447-453, 2000.
53. Marcora S. Counterpoint: Afferent feedback from fatigued locomotor muscles is not an important determinant of endurance exercise performance. J Appl Physiol 108: 454-456, 2010.
54. Marcora SM, Staiano W. The limit to exercise tolerance in humans: mind over muscle? Eur J Appl Physiol 109: 763-770, 2010.
55. Merletti R, di Torino P. Standards for reporting EMG data. J Electromyogr Kinesiol 9: III-IV, 1999.
56. Merton PA. Voluntary strength and fatigue. J Physiol 123: 553-564, 1954.
57. Millet GY. Can neuromuscular fatigue explain running strategies and performance in ultra-marathons? The flush model. Sports Med 41: 489-506, 2011.
58. Noakes TD. Fatigue is a brain-derived emotion that regulates the exercise behavior to ensure the protection of whole body homeostasis. Front Physiol 3: 82, 2012.
59. Noakes TD. Linear relationship between the perception of effort and the duration of constant load exercise that remains. J Appl Physiol 96: 1571-1572, 2004.
60. Noakes TD, Marino FE. Arterial oxygenation, central motor output and exercise performance in humans. J Physiol 585: 919-921, 2007.
61. Nordsborg N, Mohr M, Pedersen LD, Nielsen JJ, Langberg H, Bangsbo J. Muscle interstitial potassium kinetics during intense exhaustive exercise: effect of previous arm exercise. Am J Physiol Regul Integr Comp Physiol 285: R143-R148, 2003.
62. O'Donnell DE, Banzett RB, Carrieri-Kohlman V, Casaburi R, Davenport PW, Gandevia SC, Gelb AF, Mahler DA, Webb KA. Pathophysiology of dyspnea in chronic obstructive pulmonary disease: a roundtable. Proc Am Thorac Soc 4: 145-168, 2007.
63. Oskouei MA, Van Mazijk BC, Schuiling MH, Herzog W. Variability in the interpolated twitch torque for maximal and submaximal voluntary contractions. J Appl Physiol 95: 1648-1655, 2003.
64. Pires FO, Noakes TD, Lima-Silva AE, Bertuzzi R, Ugrinowitsch C, Lira FS, Kiss MA. Cardiopulmonary, blood metabolite and rating of perceived exertion responses to constant exercises performed at different intensities until exhaustion. Br J Sports Med 45: 1119-1125, 2011.
65. Rainoldi A, Melchiorri G, Caruso I. A method for positioning electrodes during surface EMG recordings in lower limb muscles. J Neurosci Methods 134: 37-43, 2004.
66. Romer LM, Haverkamp HC, Amann M, Lovering AT, Pegelow DF, Dempsey JA. Effect of acute severe hypoxia on peripheral fatigue and endurance capacity in healthy humans. Am J Physiol Regul Integr Comp Physiol 292: R598-R606, 2007.
67. Romer LM, Lovering AT, Haverkamp HC, Pegelow DF, Dempsey JA. Effect of inspiratory muscle work on peripheral fatigue of locomotor muscles in healthy humans. J Physiol 571: 425-439, 2006.
68. Rossman MJ, Garten RS, Venturelli M, Amann M, Richardson RS. The role of active muscle mass in determining the magnitude of peripheral fatigue during dynamic exercise. Am J Physiol Regul Integr Comp Physiol 306: R934-R940, 2014.
69. Sidhu SK, Weavil JC, Venturelli M, Garten RS, Rossman MJ, Richardson RS, Gmelch BS, Morgan DE, Amann M. Spinal mu-opioid receptor-sensitive lower limb muscle afferents determine corticospinal responsiveness and promote central fatigue in upper limb muscle. J Physiol 592: 5011-5024, 2014.
70. St. Clair Gibson A, Baden DA, Lambert MI, Lambert EV, Harley YX, Hampson D, Russell VA, Noakes TD. The conscious perception of the sensation of fatigue. Sports Med 33: 167-176, 2003.
71. St. Clair Gibson A, Schabort EJ, and Noakes TD. Reduced neuromuscular activity and force generation during prolonged cycling. Am J Physiol Regul Integr Comp Physiol 281: R187-R196, 2001.
72. Suter E, Herzog W. Effect of number of stimuli and timing of twitch application on variability in interpolated twitch torque. J Appl Physiol 90: 1036-1040, 2001.
73. Taylor BJ, Romer LM. Effect of expiratory muscle fatigue on exercise tolerance and locomotor muscle fatigue in healthy humans. J Appl Physiol 104: 1442-1451, 2008.
74. Taylor JL, Gandevia SC. A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104: 542-550, 2008.
75. Tucker R, Marle T, Lambert EV, Noakes TD. The rate of heat storage mediates an anticipatory reduction in exercise intensity during cycling at a fixed rating of perceived exertion. J Physiol 574: 905-915, 2006.
76. Ulmer HV. Concept of an extracellular regulation of muscular metabolic rate during heavy exercise in humans by psychophysiological feedback. Experientia 52: 416-420, 1996.
77. Vanhatalo A, Fulford J, DiMenna FJ, Jones AM. Influence of hyperoxia on muscle metabolic responses and the power-duration relationship during severe-intensity exercise in humans: a31 P magnetic resonance spectroscopy study. Exp Physiol 95: 528-540, 2010.
78. Williamson JW. The relevance of central command for the neural cardiovascular control of exercise. Exp Physiol 95: 1043-1048, 2010.
79. Wuthrich TU, Eberle EC, Spengler CM. Locomotor and diaphragm muscle fatigue in endurance athletes performing time-trials of different durations. Eur J Appl Physiol 114: 1619-1633, 2014.
80. Wuthrich TU, Notter DA, Spengler CM. Effect of inspiratory muscle fatigue on exercise performance taking into account the fatigue-induced excess respiratory drive. Exp Physiol 98: 1705-1717, 2013.