Hostname: page-component-848d4c4894-wg55d Total loading time: 0 Render date: 2024-05-17T04:27:34.280Z Has data issue: false hasContentIssue false

Le rôle joué par les fibres afférentes métabosensibles dans les mécanismes adaptatifs neuromusculaires

Published online by Cambridge University Press:  16 December 2016

Patrick Decherchi*
Affiliation:
Laboratoire des Déterminants Physiologiques de l'Activité Physique (UPRES EA 3285), Institut Fédératif de Recherches Etienne-Jules MAREY (IFR107), Faculté des Sciences du Sport de Marseille-Luminy, Case Postale 910, Université de la Méditerranée (Aix-Marseille II), Marseille, France
Erick Dousset
Affiliation:
Laboratoire des Déterminants Physiologiques de l'Activité Physique (UPRES EA 3285), Institut Fédératif de Recherches Etienne-Jules MAREY (IFR107), Faculté des Sciences du Sport de Marseille-Luminy, Case Postale 910, Université de la Méditerranée (Aix-Marseille II), Marseille, France
*
Laboratoire des Déterminants Physiologiques de l'Activité Physique (UPRES EA 3285), Institut Fédératif de Recherches Etienne-Jules MAREY (IFR107), Faculté des Sciences du Sport de Marseille-Luminy, Case Postale 910, Université de la Méditerranée (Aix-Marseille II), 163, avenue de Luminy, 13288 Marseille Cedex 09, France
Rights & Permissions [Opens in a new window]

Résumé:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Les adaptations de l'organisme à l'exercice sont permises par l'ajustement de l'activité des neurones centraux qui est en partie régulée par l'activité des afférences I et II (mécanosensibles), par la mise en jeu des afférences III et IV (métabosensibles) et par les modifications du métabolisme musculaire au cours de l'exercice. Le rôle des afférences métabosensibles apparaît comme fondamental dans les mécanismes adaptatifs à l'exercice et dans la tolérance à la fatigue. Néanmoins, de nombreuses interrogations demeurent. Cette revue fait le bilan des connaissances concernant l'implication de ces afférences dans les boucles de rétrocontrôle sensori-motrices et les mécanismes d'adaptation neuromusculaire. Il semble désormais établi que l'activation des afférences métabosensibles soit à l'origine de l'adaptation cardiovasculaire et respiratoire à l'exercice. De plus, ces afférences seraient à l'origine d'un mécanisme de protection du muscle contre la fatigue en modulant la commande motrice centrale au niveau spinal et supraspinal.

Abstract:

ABSTRACT:

Adaptation to exercise is provided by central neuron activity adjustments which are regulated partly by activation of group I and II (mechanosensitive) and group III and IV (metabosentitive) afferent fibers. These last two groups are activated by exercise-induced changes in muscle metabolism. The role played by these afferents seems to be crucial to exercise and fatigue tolerance adaptive mechanisms. Nevertheless, many questions remain unresolved. The aim of this review is to focus on the involvement of metabosensitivity in sensorimotor loops and neuromuscular adaptive mechanisms. The existence of an adaptive cardiovascular and respiratory reflex to exercise originating from metabosensitive afferent fiber activation is well established. Furthermore, the mechanism of skeletal muscle protection against fatigue could be due to modulation of central motor command at the spinal and supraspinal levels via these afferent fibers.

Type
Review Article
Copyright
Copyright © The Canadian Journal of Neurological 2003

References

RÉFÉRENCES

1. McCloskey, DI, Mitchell, JH. Reflex cardiovascular and respiratory responses originating in exercising muscle. J Physiol (Lond) 1972; 224: 173186.Google Scholar
2. Enoka, RM, Stuart, DG. Neurobiology of muscle fatigue. J Appl Physiol 1992; 72: 16311648.Google Scholar
3. Gandevia, SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001; 81:17251789.Google Scholar
4. Brown, MC, Engberg, I, Matthews, PBC. The relative sensitivity to vibration of muscle receptors of the cat. J Physiol (Lond) 1967;192:773800.Google Scholar
5. Burke, D, Hagbarth, KE, Lófstedt, L, Wallin, BG. The response of human muscle spindle endings to vibrations of non contracting muscles. J Physiol (Lond) 1976; 261:673693.Google Scholar
6. Graham, R, Jammes, Y, Delpierre, S, Grimaud, C, Roussos, CH. The effects of ischemia lactic acid and hypertonic sodium chloride on phrenic afferent discharge during spontaneous diaphragmatic contraction. Neurosci Lett 1986; 67: 257262.Google Scholar
7. Jammes, Y, Balzamo, E. Changes in afferent and efferent phrenic activities with electrically induced diaphragmatic fatigue. J Appl Physiol 1992; 73(3): 894902.Google Scholar
8. Brooks, GA. Lactic acid production under fully aerobic conditions: The lactate shuttle during rest and exercise. Fed Proc 1986; 45:29242929.Google ScholarPubMed
9. Marcos, E, Ribas, J. Kinetics of plasma potassium concentrations during exhausting exercise in trained and untrained men. Eur J Appl Physiol 1995; 71: 207214.CrossRefGoogle ScholarPubMed
10. Sjogaard, G. Role of exercise-induced potassium fluxes underlying muscle fatigue: a brief review. Can J Physiol Pharmacol 1991;69:238245.CrossRefGoogle ScholarPubMed
11. Sjogaard, G. Potassium and fatigue: the pros and cons. Acta Physiol Scand 1996; 156: 257264.Google Scholar
12. Shek, PN, Shephard, RJ. Physical exercise as a human model of limited inflammatory response. Can J Physiol Pharmacol 1998;76: 589597.Google Scholar
13. Tidball, JG. Inflammatory cell response to acute muscle injury. Med Sci Sports Exerc 1995; 27:10221032.Google Scholar
14. Sjodin, B, Westing, YH, Apple, FS. Biochemical mechanisms for oxygen free radical formation during exercise. Sports and Medicine 1990; 10: 236254.Google Scholar
15. Mense, S. Slowly conducting afferent fibers from deep tissues neurobiological properties and central nervous actions. In: Ottoson, D (Ed). Progress in Sensory Physiology. Berlin: Springer-Verlag. 1986; 6:139219.Google Scholar
16. Mitchell, JH, Schmidt, RF. Cardiovascular reflex control by afferent fibers from skeletal muscle receptors. In: Handbook of Physiology. Washington, DC: American Physiological Society. 1983.Google Scholar
17. Jammes, Y, Speck, DF. Respiratory control by diaphragmatic and respiratory afferents. In: Dempsey, JA, Pack, AI (Eds). Regulation of Breathing. Second ed. Dekker, Marcel, Inc. New York, Basel, Hong Kong; 1995.Google Scholar
18. Edwards, RHT. Hypotheses of peripheral and central mechanisms underlying occupational muscle pain and injury. Eur J Appl Physiol 1988; 57: 275281.Google Scholar
19. Paintal, AS. Functional analysis of group III afferent fibres of mammalian muscles. J Physiol 1960; 152: 250270.Google Scholar
20. Eccles, RM, Lundberg, A. Synaptic actions in motoneurones by afferents which evoke the flexion reflex. Arch Ital Biol 1959; 97:199221.Google Scholar
21. Kaufman, MP, Longhurst, JC, Rybicki, KJ, Wallach, JH, Mitchell, JH. Effects of static muscular contraction on impulse activity of group III and IV afferents in cats. J Appl Physiol 1983; 55: 105112.Google Scholar
22. Kaufman, MP, Rybicki, KJ, Waldrop, TG, Mitchell, JH. Effect on arterial pressure of rhythmically contracting the hindlimb muscles of cats. J Appl Physiol 1984; 56: 12651271.Google Scholar
23. Kaufman, MP, Rybicki, KJ, Waldrop, TG, Ordway, GA. Effects of ischemia in responses of group III and IV afferents to contraction. J Appl Physiol 1984; 57: 644650.Google Scholar
24. Kaufman, MP, Rybicki, KJ, Waldrop, TG, Ordway, GA, Mitchell, JH. Effects of static and rhythmic twitch contractions on the discharge of group III and IV muscle afferents. Cardiovasc Res 1984; 18: 663668.Google Scholar
25. Mense, S, Meyer, H. Different types of slowly conducting afferent units in cat skeletal muscle and tendon. J Physiol (Lond) 1985;363: 403417.Google Scholar
26. Hertel, HC, Howald, B, Mense, S. Responses of group IVand group III muscle afferents to thermal stimuli. Brain Res 1976; 113: 201205.Google Scholar
27. Lagier-Tessonier, F, Balzamo, E, Jammes, Y. Comparative effects of ischemia and acute hypoxemia on muscle afferents from tibialis anterior in cats. Muscle Nerve 1993; 16: 135141.Google Scholar
28. Mense, S, Stahnke, M. Responses in muscle afferent fibers of slow conduction velocity to contractions and ischemia in the cat. J Physiol (Lond) 1983; 342: 383397.Google Scholar
29. Hill, JM, Pickar, JG, Parrish, MD, Kaufman, MP. Effects of hypoxia on the discharge of group III and IV muscle afferents in cats. J Appl Physiol 1992; 73: 25242529.CrossRefGoogle ScholarPubMed
30. Kaufman, MP, Iwamoto, GA, Longhurst, JC, Mitchell, JH. Effect of capsaicin and bradykinin on afferent fibers with endings in skeletal muscle. Circ Res 1982; 50: 133139.Google Scholar
31. Rotto, D, Kaufman, MP. Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J Appl Physiol 1988; 64: 23062313.Google Scholar
32. Kenagy, J, Vancleave, J, Pazdernik, L, Orr, JA. Stimulation of group III and IV afferent nerves from the hindlimb by thromboxane A2. Brain Res 1997; 744: 175178.Google Scholar
33. Sinoway, L, Prophet, S, Gorman, I, et al. Muscle acidosis during static exercise is associated with calf vasoconstriction. J Appl Physiol 1989; 66: 429436.Google Scholar
34. Steinhagen, C, Hirchie, HJ, Nestle, W, Bovenkamp, U, Hosselmann, I. The interstitial pH of the working gastrocnemius muscle of the dog. Pluegers Arch 1976; 367: 151156.CrossRefGoogle ScholarPubMed
35. Victor, R, Bertocci, LA, Pryor, SL, Nunnally, RL. Sympathetic nerve discharge is coupled to muscle pH during exercise in humans. J Clin Invest 1988; 82: 13011305.Google Scholar
36. Herbaczynska-Cedro, K, Staszewska-Barczak, J, Janczewska, H. Muscular work and the release of prostaglandin substances. Cardiovasc Res 1976; 10: 413420.Google Scholar
37. Stebbins, CL, Maruoka, Y, Longhurst, JC. Prostaglandins contribute to cardiovascular reflexes evoked by static muscular contraction. Circ Res 1986; 59: 645654.CrossRefGoogle ScholarPubMed
38. Hnìk, P, Hudlická, J, Kucera, J, Payne, R. Activation of muscle afferents by nonproprioceptive stimuli. Am J Physiol 1969; 217: 14511457.Google Scholar
39. Kaufman, MP, Rybicki, KJ. Discharge properties of group III and IV muscle afferents: their responses to mechanical and metabolic stimuli. Circ Res 1987; 61(Suppl): I60–I65.Google Scholar
40. Rybicki, KJ, Waldrop, TG, Kaufman, MP. Increasing gracilis muscle interstitial potassium concentrations stimulate group III and IV afferents. J Appl Physiol 1985; 58: 936941.Google Scholar
41. Rotto, DM, Massey, KD, Burton, KP, Kaufman, MP. Static contraction increases arachidonic acid levels in gastrocnemius muscles of cats. J Appl Physiol 1989; 66: 27212724.Google Scholar
42. Thimm, F, Baum, K. Response of chemosensitive nerve fibers of group III and IV to metabolic changes in rat muscles. Pfluegers Arch 1987; 410: 143152.Google Scholar
43. Vollestad, NK, Sejersted, DM. Biochemical correlates of fatigue. Eur J Appl Physiol 1988; 57: 336347.Google Scholar
44. Westra, HG, De Haan, A, Van Doorn, JE, De Hann, EJ. Anaerobic chemical changes and mechanical outpout during isometric tetani of rat skeletal muscle in situ. Pfluegers Arch 1988; 412: 121127.Google Scholar
45. Hayward, L, Wesselmann, U, Rymer, WZ. Effects of muscle fatigue on mechanically sensitive afferents of slow conduction velocity in the cat triceps surae. J Neurophysiol 1991; 65: 360370.Google Scholar
46. 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 1998; 257: 14.Google Scholar
47. Decherchi, P, Darques, JL, Jammes, Y. Modifications of afferent activities from tibialis anterior muscle in rat by tendon vibrations, increase of interstitial potassium or lactate concentration and electrically induced fatigue. J Periph Nerv System 1998; 3: 110.Google Scholar
48. Darques, JL, Jammes, Y. Fatigue induced changes in group IV muscle afferent activity: differences between high and low frequency electrically induced fatigue. Brain Res 1997; 750: 109112.Google Scholar
49. Garland, SJ. Role of small diameter afferents in reflex inhibition during human muscle fatigue. J Physiol 1991; 435: 547558.Google Scholar
50. Kao, FF. An experimental study of the pathway involved in exercise hyperpnoea employing cross-circulation techniques. In: Cunningham, DJC, Llyod, BB (Eds). The Regulation of Human Respiration. Oxford: Blackwell Scientific Publications 1963;461502.Google Scholar
51. Coote, JH, Hilton, SM, Pérez-Gonzàlez, JF. The reflex nature of the pressor response to muscular exercise. J Physiol 1971; 215: 789804.Google Scholar
52. Stegemann, J, Kenner, TH. A theory on heart rate control by muscular metabolic receptors. Arch Kreisl 1971; Forsch 64: 185214.Google Scholar
53. Pérez-Gonzàlez, JF, Coote, JH. Activity of muscle afferents and reflex circulatory responses to exercise. Am J Physiol 1972; 221:138143.Google Scholar
54. Dejours, P. Control of respiration in muscular exercise. In: Fenn, WO, Rahn, H, (Eds). Handbook of Physiology, section 3: Respiration, vol. 1. Washington DC: American Physiology Society 1964; 631648.Google Scholar
55. Asmussen, E. Muscle fatigue. Med Sci Sports Exerc 1979; 25(4): 411420.Google Scholar
56. Edwards, RG Lippold, OC. The relation between force and integrated electrical activity in fatigue muscle. J Physiol (Lond) 1956; 132:677681.Google Scholar
57. Simonson, E. Physiology of work capacity and fatigue. Springfield, IL: Thomas, 1971.Google Scholar
58. Edwards, RH, Round, JM, Jones, DA. Needle biopsy of skeletal muscle: a review of 10 years experience. Muscle Nerve 1983; 6:676683.Google Scholar
59. Bigland-Ritchie, B, Woods, JJ. Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 1984; 7: 691699.Google Scholar
60. Bigland-Ritchies, B. EMG and fatigue of human voluntary and stimulated contractions. Ciba Foundation Symposium 1981; 82:130156.Google Scholar
61. Gollhofer, A, Komi, PV, Fujitsuka, N, Miyashita, M. Fatigue during stretch-shortening cycle exercises. II. Changes in neuromuscular activation patterns of human skeletal muscle. Int J Sports Med 1987; 8: 3847.Google Scholar
62. Bigland-Ritchie, B, Lippold, OCJ. Changes in muscle activation during prolonged maximal voluntary contractions. J Physiol (Lond) 1979; 292: 1415.Google Scholar
63. Bigland-Ritchie, BR, Dawson, NJ, Johansson, RS, Lippold, OCJ. Reflex origin for the slowing of motoneurone firing rates in fatigue of human voluntary contraction. J Physiol (Lond) 1986; 379: 451459.Google Scholar
64. Fitts, RH. Cellular mechanisms of muscle fatigue. Physiol Rev 1994; 74: 4994.Google Scholar
65. Alam, M, Smirk, FH. Observation in man upon a blood pressure raising reflex arising from the voluntary muscle. J Physiol 1937;89: 372383.Google Scholar
66. Vanbenthuysen, KM, Swanson, GD, Weil, JV. Temporal delay of venous blood correlates with onset of exercise hypernea. Appl Physiol 1984; 54: 874880.Google Scholar
67. Adams, L, Frankel, H, Garlick, J, Guz, A, Murphy, K, Semple, SJG. The role of spinal cord transmission in the ventilatory response to exercise in man. 1984; 355: 8597.Google Scholar
68. Goodwin, GM, McCloskey, DI, Mitchell, JH. Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension. J Physiol 1972;226: 173190.CrossRefGoogle ScholarPubMed
69. Eldridge, FL, Millhorn, DE, Waldrop, TG. Exercise hypernea and locomotion: parallel activation from hypothalamus. Science 1981; 211: 844846.Google Scholar
70. Shepherd, JT, Blomqvist, CG, Lind, AR, Mitchell, JH, Saltin, B. Static (isometric) exercise. Circ Res 1981; 48(Suppl 1):I179–I188.Google Scholar
71. Mitchell, JH, Reardon, WC, McCloskey, KI. Reflex effect on circulation and respiration from contracting skeletal muscle. Am J Physiol 1977; 233: H374–H378.Google Scholar
72. Clement, DL. Neurogenic influences on blood pressure and vascular tone from peripheral receptors during muscular contraction. Cardiology 1976; 61 (Suppl 1): 6568.Google Scholar
73. Fisher, M, Nutter, DO. Cardiovascular reflex adjustments to static muscular contractions in the canine hindlimb. Am J Physiol 1974;226(3): 648655.Google Scholar
74. Coote, JH, Pérez-Gonzàlez, JF. The response of some sympathetic neurones to volleys in various afferent nerves. J Physiol 1970;208: 261278.Google Scholar
75. Asmussen, E, Nielsen, M. Experiments on nervous factors controlling respiration and circulation during muscular exercise employing blocking of the blood flow. Acta Physiol Scand 1964;60: 103111.Google Scholar
76. Staunton, HP, Taylor, SH, Donald, KW. Effect of vascular occlusion on the pressor responses to static muscular work. Clin Sci 1964;27: 283291.Google Scholar
77. Mitchell, JH, Kaufman, MP, Iwamoto, GA. The exercise pressor reflex: its cardiovascular effects, afferent mechanisms and central pathways. Ann Rev Physiol 1983; 45: 229242.Google Scholar
78. Ramsay, AG. Effects of metabolism and anesthesia on pulmonary ventilation. J Appl Physiol 1959; 14: 102104.Google Scholar
79. Rein, H. Die inter Ferenz der vasomotorrischen Regulation. Klin Wochenschr 1930; 9: 14851489.Google Scholar
80. Kohrman, RM, Nolasco, JB, Wiggers, CJ. Types of afferent fibers in the phrenic nerve. Am J Physiol 1947; 151: 547553.CrossRefGoogle ScholarPubMed
81. McCallister, LW, McCoy, KW, Connelly, JC, Kaufman, MP. Stimulation of group III and IV phrenic afferents reflexly decreases total lung resistance in dogs. J Appl Physiol 1986; 61: 13461351.Google Scholar
82. Suspinski, GS, Stofan, TDD, Dimarco, AF. Effect of intraphrenic injection of potassium on diaphragm activation. J Appl Physiol 1993; 74(3): 11861194.CrossRefGoogle Scholar
83. Jammes, Y, Buchler, B, Delpierre, S, Rasidakis, A, Grimaud, C, Roussos, C. Phrenic afferents and their role in inspiratory control. J Appl Physiol 1986; 60: 854860.Google Scholar
84. Speck, DF. Supraspinal involvement in the phrenic-to-phrenic inhibitory reflex. Brain Res 1987; 414: 169172.Google Scholar
85. Speck, DF, Revelette, WR. Attenuation of phrenic motor discharge by phrenic nerve afferents. J Appl Physiol 1987; 62: 941945.Google Scholar
86. Suspinski, GS, Dimarco, AF, Hussein, F, Altose, MD. Alterations in respiratory muscle activation in the ischemic fatigued canine diaphragm. J Appl Physiol 1989; 67: 720729.Google Scholar
87. Burnet, H, Lenoir, P, Jammes, Y. Changes in respiratory muscle activity in conscious cats during experimental dives at 101 ATA. J Appl Physiol 1992; 73:465472.Google Scholar
88. Aubier, M, Trippenbach, T, Roussos, C. Respiratory muscle fatigue during cardiogenic shock. J Appl Physiol 1981; 51: 499508.Google Scholar
89. Roussos, C. Ventilatory muscle fatigue governs breathing frequency. Clin Respir Physiol 1984; 20: 445451.Google Scholar
90. Gallagher, CG, Im Hof, V, Younes, M. Effect of inspiratory muscle fatigue on breathing pattern. J Appl Physiol 1985; 59: 11521158.Google Scholar
91. Mador, MJ, Acevedo, FA. Effect of inspiratory muscle fatigue on breathing pattern during inspiratory resistive loading. J Appl Physiol 1991; 70: 16271632.Google Scholar
92. Woods, JJ, Furbush, F, Bigland-Ritchie, B. Evidence for a fatigue- induced reflex inhibition of motoneuron firing rates. J Neurophysiol 1987; 58: 125137.Google Scholar
93. Dousset, E, Decherchi, P, Grelot, L Jammes, Y. Effects of chronic hypoxemia on the afferent nerve activities from skeletal muscle. Am J Respir Crit Care Med 2001; 164: 14761480.Google Scholar
94. Dousset, E, Decherchi, P, Grelot, L, Jammes, Y. Comparison between acute and chronic hypoxemia effects on muscle afferent activities from tibialis anterior muscle. Exp Brain Res 2003;148:320327.CrossRefGoogle ScholarPubMed
95. Dousset, E, Steinberg, JG, Balon, N, Jammes, Y. Effects of acute hypoxemia on force and surface EMG during sustained handgrip. Muscle Nerve 2001; 24: 364371.Google Scholar
96. Caquelard, F, Burnet, H, Tagliarini, F, et al. Effects of prolonged hypobaric hypoxia on human skeletal muscle function and electromyographic events. Clin Sci 2000; 98: 329337.Google Scholar
97. Faulkner, JA, Brooks, SV, Opiteck, JA. Injury to skeletal muscle fibers during contractions: conditions of occurrence and prevention. Phys Ther 1993; 73:911921.Google Scholar
98. 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; 1:1017.Google Scholar