Somatosensory feedback from the limbs exerts inhibitory influences on central neural drive during whole body endurance exercise

Journal of Applied Physiology

Volumn 105, Issue 6, 2008, Pages 1714-1724

  Amann, Markus ^a,b   Proctor, Lester T ^a   Sebranek, Joshua J ^a   Eldridge, Marlowe W ^a   Pegelow, David F ^a   Dempsey, Jerome A ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Ascending sensory pathway; Cardiorespiratory response; Control of breathing; Exercise hyperpnea; Muscle metaboreflex; Nociception

Indexed keywords

CARBON DIOXIDE;

ADULT; ARTICLE; BLOOD PRESSURE; CENTRAL NERVOUS SYSTEM FUNCTION; CYCLING; ELECTROMYOGRAM; ENDURANCE; EPIDURAL ANESTHESIA; EXERCISE; FAST MUSCLE; FEEDBACK SYSTEM; HEART RATE; HUMAN; HUMAN EXPERIMENT; LEG MUSCLE; MALE; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE TWITCH; NORMAL HUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; SOMATOSENSORY STIMULATION; VASTUS LATERALIS MUSCLE; VOLUNTARY MOVEMENT;

EID: 57349200600     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.90456.2008     Document Type: Article

References (85)

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. Amann M, Calbet JA. Convective oxygen transport and fatigue. J Appl Physiol 104: 861-870, 2008.
3. 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.
4. Amann M, Eldridge MW, Lovering AT, Stickland MK, Pegelow DF, Dempsey JA. Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue. J Physiol 575: 937-952, 2006.
5. Amann M, Hopkins WG, Marcora SM. Similar sensitivity of time to exhaustion and time trial to changes in endurance. Med Sci Sports Exerc 40: 574-578, 2008.
6. Amann M, Pegelow DF, Jacques AJ, Dempsey JA. Inspiratory muscle work in acute hypoxia influences locomotor muscle fatigue and exercise performance of healthy humans. Am J Physiol Regul Integr Comp Physiol 293: R2036-R2045, 2007.
7. Amann M, Romer L, Dempsey J. To the Editor. Response to Noakes' Letter to the Editor. J Physiol 585: 923-924, 2007.
8. 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.
9. 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.
10. Amann M, Subudhi A, Foster C. Influence of testing protocol on ventilatory thresholds and cycling performance. Med Sci Sports Exerc 36: 613-622, 2004.
11. Arendt-Nielsen L, Mills KR. The relationship between mean power frequency of the EMG spectrum and muscle fibre conduction velocity. Electroencephalogr Clin Neurophysiol 60: 130-134, 1985.
12. Asmussen E, Johansen SH, Jorgensen M, Nielsen M. On the nervous factors controlling respiration and circulation during exercise. Experiments with curarization. Acta Physiol Scand 63: 343-350, 1965.
13. 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.
14. Borg G. Borg's Perceived Exertion and Pain Scales. Champaign, IL: Human Kinetics, 1998.
15. Brennum J. Quantitative sensory examination of epidural anaesthesia and analgesia in man. Acta Physiol Scand Suppl 634: 1-27, 1996.
16. Bromage PR. Mechanism of action of extradural analgesia. Br J Anaesth Suppl 47: 199-211, 1975.
17. Butterworth JF, Strichartz GR. Molecular mechanisms of local anesthesia: a review. Anesthesiology 72: 711-734, 1990.
18. Caquelard F, Burnet H, Tagliarini F, Cauchy E, Richalet JP, Jammes Y. Effects of prolonged hypobaric hypoxia on human skeletal muscle function and electromyographic events. Clin Sci (Lond) 98: 329-337, 2000.
19. Chavarren J, Calbet JA. Cycling efficiency and pedalling frequency in road cyclists. Eur J Appl Physiol 80: 555-563, 1999.
20. Dalsgaard MK, Ide K, Cai Y, Quistorff B, Secher NH. The intent to exercise influences the cerebral O(2)/carbohydrate uptake ratio in humans. J Physiol 540: 681-689, 2002.
21. Dela F, Mohr T, Jensen CM, Haahr HL, Secher NH, Biering-Sorensen F, Kjaer M. Cardiovascular control during exercise: insights from spinal cord-injured humans. Circulation 107: 2127-2133, 2003.
22. Duhamel TA, Green HJ, Sandiford SD, Perco JG, Ouyang J. Effects of progressive exercise and hypoxia on human muscle sarcoplasmic reticulum function. J Appl Physiol 97: 188-196, 2004.
23. Edgerton VR, Roy RR. The nervous system and movement. In: ACSM's Advanced Exercise Physiology, edited by Tipton CM. Philadelphia: Lippincott Williams & Wilkins, 2006, p. 41-94.
24. Eldridge FL, Millhorn DE, Kiley JP, Waldrop TG. Stimulation by central command of locomotion, respiration and circulation during exercise. Respir Physiol 59: 313-337, 1985.
25. Eldridge FL, Millhorn DE, Waldrop TG. Exercise hyperpnea and locomotion: parallel activation from the hypothalamus. Science 211: 844-846, 1981.
26. Enoka RM, Stuart DG. Neurobiology of muscle fatigue. J Appl Physiol 72: 1631-1648, 1992.
27. Farina D, Macaluso A, Ferguson RA, De Vito G. Effect of power, pedal rate, and force on average muscle fiber conduction velocity during cycling. J Appl Physiol 97: 2035-2041, 2004.
28. Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol 96: 1486-1495, 2004.
29. Fernandes A, Galbo H, Kjaer M, Mitchell JH, Secher NH, Thomas SN. Cardiovascular and ventilatory responses to dynamic exercise during epidural anaesthesia in man. J Physiol 420: 281-293, 1990.
30. Fink BR. Mechanism of differential epidural block. Anesth Analg 65: 325-329, 1986.
31. Fink BR. Mechanisms of differential axial blockade in epidural and subarachnoid anesthesia. Anesthesiology 70: 851-858, 1989.
32. Fitts RH. Cellular mechanisms of muscle fatigue. Physiol Rev 74: 49-94, 1994.
33. Friedman DB, Brennum J, Sztuk F, Hansen OB, Clifford PS, Bach FW, Arendt-Nielsen L, Mitchell JH, Secher NH. The effect of epidural anaesthesia with 1% lidocaine on the pressor response to dynamic exercise in man. J Physiol 470: 681-691, 1993.
34. Galbo H, Kjaer M, Secher NH. Cardiovascular, ventilatory and catecholamine responses to maximal dynamic exercise in partially curarized man. J Physiol 389: 557-568, 1987.
35. Gandevia SC. Neural control in human muscle fatigue: changes in muscle afferents, motoneurones and motor cortical drive. Acta Physiol Scand 162: 275-283, 1998.
36. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81: 1725-1789, 2001.
37. Graven-Nielsen T, Lund H, Arendt-Nielsen L, Danneskiold-Samsoe B, Bliddal H. Inhibition of maximal voluntary contraction force by experimental muscle pain: a centrally mediated mechanism. Muscle Nerve 26: 708-712, 2002.
38. Grouls R, Korsten E, Ackerman E, Hellebrekers L, van Zundert A, Breimer D. Diffusion of n-butyl-p-aminobenzoate (BAB), lidocaine and bupivacaine through the human dura-arachnoid mater in vitro. Eur J Pharm Sci 12: 125-131, 2000.
39. Hargreaves M. Fatigue mechanisms determining exercise performance: integrative physiology is systems biology. First published January 31 2008; doi:101152.00088.02008.
40. Harms CA, McClaran SR, Nickele GA, Pegelow DF, Nelson WB, Dempsey JA. Exercise-induced arterial hypoxaemia in healthy young women. J Physiol 507: 619-628, 1998.
41. Hautier CA, Linossier MT, Belli A, Lacour JR, Arsac LM. Optimal velocity for maximal power production in non-isokinetic cycling is related to muscle fibre type composition. Eur J Appl Physiol 74: 114-118, 1996.
42. Hogan MC, Richardson RS, Haseler LJ. Human muscle performance and PCr hydrolysis with varied inspired oxygen fractions: a 31P-MRS study. J Appl Physiol 86: 1367-1373, 1999.
43. Hogan MC, Welch HG. Effect of varied lactate levels on bicycle ergometer performance. J Appl Physiol 57: 507-513, 1984.
44. Innes JA, De Cort SC, Evans PJ, Guz A. Central command influences cardiorespiratory response to dynamic exercise in humans with unilateral weakness. J Physiol 448: 551-563, 1992.
45. Katayama K, Amann M, Pegelow DF, Jacques AJ, Dempsey JA. Effect of arterial oxygenation on quadriceps fatigability during isolated muscle exercise. Am J Physiol Regul Integr Comp Physiol 292: R1279-R1286, 2007.
46. Kaufman MP, Longhurst JC, Rybicki KJ, Wallach JH, Mitchell JH. Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. J Appl Physiol 55: 105-112, 1983.
47. Keenan KG, Farina D, Maluf KS, Merletti R, Enoka RM. Influence of amplitude cancellation on the simulated surface electromyogram. J Appl Physiol 98: 120-131, 2005.
48. Kent-Braun JA. Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort. Eur J Appl Physiol Occup Physiol 80: 57-63, 1999.
49. Kjaer M, Hanel B, Worm L, Perko G, Lewis SF, Sahlin K, Galbo H, Secher NH. Cardiovascular and neuroendocrine responses to exercise in hypoxia during impaired neural feedback from muscle. Am J Physiol Regul Integr Comp Physiol 277: R76-R85, 1999.
50. Kjaer M, Secher NH, Bach FW, Galbo H, Reeves DR Jr, Mitchell JH. Hormonal, metabolic, and cardiovascular responses to static exercise in humans: influence of epidural anesthesia. Am J Physiol Endocrinol Metab 261: E214-E220, 1991.
51. Kjaer M, Secher NH, Bach FW, Sheikh S, Galbo H. Hormonal and metabolic responses to exercise in humans: effect of sensory nervous blockade. Am J Physiol Endocrinol Metab 257: E95-E101, 1989.
52. Kniffki KD, Mense S, Schmidt RF. Responses of group IV afferent units from skeletal muscle to stretch, contraction and chemical stimulation. Exp Brain Res 31: 511-522, 1978.
53. Krogh A, Lindhard J. The regulation of respiration and circulation during the initial stages of muscular work. J Physiol 47: 112-136, 1913.
54. Martin PG, Weerakkody N, Gandevia SC, Taylor JL. Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans. J Physiol 586: 1277-1289, 2008.
55. Mense S. Nervous outflow from skeletal muscle following chemical noxious stimulation. J Physiol 267: 75-88, 1977.
56. Merton PA. Voluntary strength and fatigue. J Physiol 123: 553-564, 1954.
57. Mitchell JH, Kaufman MP, Iwamoto GA. The exercise pressor reflex: its cardiovascular effects, afferent mechanisms, and central pathways. Annu Rev Physiol 45: 229-242, 1983.
58. Mitchell JH, Reeves DR Jr, Rogers HB, and Secher NH. Epidural anaesthesia and cardiovascular responses to static exercise in man. J Physiol 417: 13-24, 1989.
59. Mitchell JH, Reeves DR Jr, Rogers HB, Secher NH, Victor RG. Autonomic blockade and cardiovascular responses to static exercise in partially curarized man. J Physiol 413: 433-445, 1989.
60. Nielsen B, Nybo L. Cerebral changes during exercise in the heat. Sports Med 33: 1-11, 2003.
61. Noakes TD, Marino FE. Arterial oxygenation, central motor output and exercise performance in humans. J Physiol 585: 919-923, 2007.
62. Nybo L. CNS fatigue and prolonged exercise: effect of glucose supplementation. Med Sci Sports Exerc 35: 589-594, 2003.
63. Nybo L, Secher NH. Cerebral perturbations provoked by prolonged exercise. Prog Neurobiol 72: 223-261, 2004.
64. Ochwadt B, Bücherl E, Kreuzer H, Löschcke HH. Beeinflussung der Atemsteigerung bei Muskelarbeit durch partiellen neuromuskulären Block (Tubocurarine). Pflügers Arch 269: 613-621, 1959.
65. Petersen NT, Taylor JL, Butler JE, Gandevia SC. Depression of activity in the corticospinal pathway during human motor behavior after strong voluntary contractions. J Neurosci 23: 7974-7980, 2003.
66. Raymond SA. Effects on impulse generation and conduction in single myelinated sciatic nerve axons in frog. Anesth Analg 75: 906-921, 1992.
67. 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.
68. Rotto DM, Kaufman MP. Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J Appl Physiol 64: 2306-2313, 1988.
69. Sandiford SD, Green HJ, Duhamel TA, Schertzer JD, Perco JD, Ouyang J. Muscle Na-K-pump and fatigue responses to progressive exercise in normoxia and hypoxia. Am J Physiol Regul Integr Comp Physiol 289: R441-R449, 2005.
70. Smith SA, Querry RG, Fadel PJ, Gallagher KM, Stromstad M, Ide K, Raven PB, Secher NH. Partial blockade of skeletal muscle somatosensory afferents attenuates baroreflex resetting during exercise in humans. J Physiol 551: 1013-1021, 2003.
71. Strange S, Secher NH, Pawelczyk JA, Karpakka J, Christensen NJ, Mitchell JH, Saltin B. Neural control of cardiovascular responses and of ventilation during dynamic exercise in man. J Physiol 470: 693-704, 1993.
72. Strojnik V, Komi PV. Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol 84: 344-350, 1998.
73. Thornton JM, Guz A, Murphy K, Griffith AR, Pedersen DL, Kardos A, Leff A, Adams L, Casadei B, Paterson DJ. Identification of higher brain centres that may encode the cardiorespiratory response to exercise in humans. J Physiol 533: 823-836, 2001.
74. Thorstensson A, Grimby G, Karlsson J. Force-velocity relations and fiber composition in human knee extensor muscles. J Appl Physiol 40: 12-16, 1976.
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. Usubiaga JE, Wikinski J, Wikinski R, Usubiaga LE, Pontremoli M. Transfer of Local Anesthetics to the Subarachnoid Space and Mechanisms of Epidural Block. Anesthesiology 25: 752-759, 1964.
77. Victor RG, Pryor SL, Secher NH, Mitchell JH. Effects of partial neuromuscular blockade on sympathetic nerve responses to static exercise in humans. Circ Res 65: 468-476, 1989.
78. Victor RG, Secher NH, Lyson T, Mitchell JH. Central command increases muscle sympathetic nerve activity during intense intermittent isometric exercise in humans. Circ Res 76: 127-131, 1995.
79. Waldrop TG, Eldridge FL, Iwamoto GA, Mitchell JH. Central neural control of respiration and circulation during exercise. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, chapt. 9, p. 333-380.
80. Waldrop TG, Iwamoto GA. Point: supraspinal locomotor centers do contribute significantly to the hyperpnea of dynamic exercise. J Appl Physiol 100: 1077-1079, 2006.
81. Williamson JW, McColl R, Mathews D, Mitchell JH, Raven PB, Morgan WP. Brain activation by central command during actual and imagined handgrip under hypnosis. J Appl Physiol 92: 1317-1324, 2002.
82. Williamson JW, Olesen HL, Pott F, Mitchell JH, Secher NH. Central command increases cardiac output during static exercise in humans. Acta Physiol Scand 156: 429-434, 1996.
83. Woods JJ, Furbush F, Bigland-Ritchie B. Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. J Neurophysiol 58: 125-137, 1987.
84. Yang JF, Winter DA. Electromyography reliability in maximal and submaximal isometric contractions. Arch Phys Med Rehabil 64: 417-420, 1983.
85. Yokoyama M, Hanazaki M, Fujii H, Mizobuchi S, Nakatsuka H, Takahashi T, Matsumi M, Takeuchi M, Morita K. Correlation between the distribution of contrast medium and the extent of blockade during epidural anesthesia. Anesthesiology 100: 1504-1510, 2004.