Group III and IV muscle afferents: Role on central motor drive and clinical implications

Neuroscience

Volumn 290, Issue , 2015, Pages 543-551

  Laurin, J ^a   Pertici, V ^a   Dousset, E ^a   Marqueste, T ^a   Decherchi, P ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Locomotion; Metabosensitive and mechanosensitive fibers; Motor unit regulation; Muscle fatigue; Sensorimotor disturbances

Indexed keywords

ALPHA NERVE FIBER; CHRONIC OBSTRUCTIVE LUNG DISEASE; ENDURANCE TRAINING; EVOKED MUSCLE RESPONSE; HEART FAILURE; HOFFMANN REFLEX; HUMAN; HYPERTENSION; KINESIOTHERAPY; LOCOMOTION; MECHANOTRANSDUCTION; MOTOR CONTROL; MUSCLE ATROPHY; MUSCLE FATIGUE; MUSCLE SPINDLE AFFERENT NERVE; NEUROPHYSIOLOGICAL RECRUITMENT; NONHUMAN; PRESSORECEPTOR REFLEX; REVIEW; SENSORY FEEDBACK; SKELETAL MUSCLE; SPINAL CORD INJURY; ANIMAL; EXERCISE; MOTONEURON; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY; SENSORY NERVE;

AFFERENT PATHWAYS; ANIMALS; EXERCISE; HUMANS; MOTOR NEURONS; MOVEMENT; MUSCLE, SKELETAL;

EID: 84923039019     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.01.065     Document Type: Review

References (108)

1. Adreani C.M., Kaufman M.P. Effect of arterial occlusion on responses of group III and IV afferents to dynamic exercise. J Appl Physiol 1998, 84:1827-1833.
2. Adreani C.M., Hill J.M., Kaufman M.P. Responses of group III and IV muscle afferents to dynamic exercise. J Appl Physiol 1997, 82:1811-1817.
3. Almeida T.F., Roizenblatt S., Tufik S. Afferent pain pathways: a neuroanatomical review. Brain Res 2004, 1000:40-56.
4. Amann M., Dempsey J.A. Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol 2008, 586:161-173.
5. Amann M., Proctor L.T., Sebranek J.J., Eldridge M.W., Pegelow D.F., Dempsey J.A. Somatosensory feedback from the limbs exerts inhibitory influences on central neural drive during whole body endurance exercise. J Appl Physiol 2008, 105:1714-1724.
6. Amann M., Proctor L.T., Sebranek J.J., Pegelow D.F., Dempsey J.A. Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 2009, 587:271-283.
7. Amann M., Blain G.M., Proctor L.T., Sebranek J.J., Pegelow D.F., Dempsey J.A. Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. J Physiol 2011, 589:5299-5309.
8. Amann M., Venturelli M., Ives S.J., McDaniel J., Layec G., Rossman M.J., Richardson R.S. Peripheral fatigue limits endurance exercise via a sensory feedback-mediated reduction in spinal motoneuronal output. J Appl Physiol 2013, 115:355-364.
9. Amann M., Venturelli M., Ives S.J., Morgan D.E., Gmelch B., Witman M.A.H., Groot H., Wray D., Stehlik J., Richardson R.S. Group III/IV muscle afferents impair limb blood in patients with chronic heart failure. Int J Cardiol 2014, 174:368-375.
10. Bement M.K., Sluka K.A. Low-intensity exercise reverses chronic muscle pain in the rat in a naloxone-dependent manner. Arch Phys Med Rehabil 2005, 86:1736-1740.
11. Bevan S., Szolcsányi J. Sensory neuron-specific actions of capsaicin: mechanisms and applications. Trends Pharmacol Sci 1990, 11:330-333.
12. 3 improves respiratory adjustment to fatigue and H-reflex responses in paraplegic adult rats. Neuroscience 2011, 188:182-192.
13. Butler J.E., Taylor J.L., Gandevia S.C. Responses of human motoneurons to corticospinal stimulation during maximal voluntary contractions and ischemia. J Neurosci 2003, 23:10224-10230.
14. Connor M., Naves L.A., McCleskey E.W. Contrasting phenotypes of putative proprioceptive and nociceptive trigeminal neurons innervating jaw muscle in rat. Mol Pain 2005, 24(1):31.
15. Decherchi P., Dousset E. Role of metabosensitive afferent fibers in neuromuscular adaptive mechanisms. Can J Neurol Sci 2003, 30:91-97.
16. Degtyarenko A.M., Kaufman M.P. Fictive locomotion and scratching inhibit dorsal horn neurons receiving thin fiber afferent input. Am J Physiol Regul Integr Comp Physiol 2000, 279:R394-R403.
17. Degtyarenko A.M., Kaufman M.P. Stimulation of the mesencephalic locomotor region inhibits the discharge of neurons in the superficial laminae of the dorsal horn of cats. Neurosci Lett 2000, 296:109-112.
18. Degtyarenko A.M., Kaufman M.P. Stimulation of the MLR inhibits the discharge of dorsal horn neurons responsive to muscular contraction. Brain Res 2000, 880:178-182.
19. Degtyarenko A.M., Kaufman M.P. Bicuculline and strychnine suppress the mesencephalic locomotor region-induced inhibition of group III muscle afferent input to the dorsal horn. Neuroscience 2003, 118:779-788.
20. Delliaux S., Brerro-Saby C., Steinberg J.G. Reactive oxygen species activate the group IV muscle afferents in resting and exercising muscle in rats. Pflugers Arch 2009, 459:143-150.
21. Detloff M.R., Smith E.J., Molina D.Q., Ganzer P.D. Acute exercise prevents the development of neuropathic pain and the sprouting of non-peptidergic (GDNF-and artemin-responsive) c-fibers after spinal cord injury. Exp Neurol 2014, 255:38-48.
22. Dousset E., Marqueste T., Decherchi P. Effects of neonatal capsaicin deafferentation on neuromuscular adjustments, performance, and afferent activities from adult tibialis anterior muscle during exercise. J Neurosci Res 2004, 76:734-741.
23. Dousset E., Avela J., Ishikawa M., Kallio J., Kuitunen S., Kyröláinen H., Linnamo V., Komi P.V. Bimodal recovery pattern in human skeletal muscle induced by exhaustive stretch-shortening cycle exercise. Med Sci Sports Exerc 2007, 39:453-460.
24. Duchateau J., Balestra C., Carpentier A., Hainaut K. Reflex regulation during sustained and intermittent submaximal contractions in humans. J Physiol 2002, 541:959-967.
25. Falla D., Farina D., Graven-Nielsen T. Experimental muscle pain results in reorganization of coordination among trapezius muscle subdivisions during repetitive shoulder flexion. Exp Brain Res 2007, 178:385-393.
26. Gagnon P., Bussières J.S., Ribeiro F., Gagnon S.L., Saey D., Gagné N., Provencher S., Maltais F. Influences of spinal anesthesia on exercise tolerance in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2012, 186:606-615.
27. Gandevia S.C. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001, 81:1725-1789.
28. Garland S.J.S. Role of small diameter afferents in reflex inhibition during human muscle fatigue. J Physiol 1991, 435:547-558.
29. Ge W., Khalsa P.S. Encoding of compressive stress during indentation by group III and IV muscle mechano-nociceptors in rat gracilis muscle. J Neurophysiol 2003, 89:785-792.
30. Gibson W., Arendt-Nielsen L., Taguchi T., Mizumura K., Graven-Nielsen T. Increased pain from muscle fascia following eccentric exercise: animal and human findings. Exp Brain Res 2009, 194:299-308.
31. Graven-Nielsen T., McArdle A., Phoenix J., Arendt-Nielsen L., Jensen T.S., Jackson M.J., Edwards R.H. In vivo model of muscle pain: quantification of intramuscular chemical, electrical, and pressure changes associated with saline-induced muscle pain in humans. Pain 1997, 69:137-143.
32. Hanna R.L., Kaufman M.P. Role played by purinergic receptors on muscle afferents in evoking the exercise pressor reflex. J Appl Physiol 2003, 94:1437-1445.
33. Hanna R.L., Kaufman M.P. Activation of thin-fiber muscle afferents by a P2X agonist in cats. J Appl Physiol 2004, 96:1166-1169.
34. Haouzi P., Hill J.M., Lewis B.K., Kaufman M.P. Responses of group III and IV muscle afferents to distension of the peripheral vascular bed. J Appl Physiol 1999, 87:545-553.
35. Hayes S.G., Kaufman M.P. Gadolinium attenuates exercise pressor reflex in cats. Am J Physiol Heart Circ Physiol 2001, 280:H2153-H2161.
36. Hayes S.G., McCord J.L., Koba S., Kaufman M.P. Gadolinium inhibits group III but not group IV muscle afferent responses to dynamic exercise. J Physiol 2009, 587:873-882.
37. Hoheisel U., Reinöhl J., Unger T., Mense S. Acidic pH and capsaicin activate mechanosensitive group IV muscle receptors in the rat. Pain 2004, 110:149-157.
38. Hu-Tsai M., Winter J., Woolf C.J. Regional differences in the distribution of capsaicin-sensitive target-identified adult rat dorsal root ganglion neurons. Neurosci Lett 1992, 143:251-254.
39. Jancso G., Kiraly E., Jancso-Gabor A. Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. Nature 1977, 270:741-743.
40. Jankowski M.P., Rau K.K., Ekmann K.M., Anderson C.E., Koerber H.R. Comprehensive phenotyping of group III and IV muscle afferents in mouse. J Neurophysiol 2013, 109:2374-2381.
41. Kalezic I., Bugaychenko L.A., Kostyukov A.I., Pilyavskii A.I., Ljubisavljevic M., Windhorst U., Johansson H. Fatigue-related depression of the feline monosynaptic gastrocnemius-soleus reflex. J Physiol 2004, 556:283-296.
42. Kalezic I., Pilyavskii A.I., Maisky V.A., Kostyukov A.I., Windhorst U., Johansson H. Distinctive pattern of c-fos expression in the feline cervico-lumbar spinal cord after stimulation of vanilloid receptors in dorsal neck muscles. Neurosci Lett 2004, 364:94-97.
43. Kalliomäki J., Luo X.L., Yu Y.B., Schouenborg J. Intrathecally applied morphine inhibits nociceptive C fiber input to the primary somatosensory cortex (SI) of the rat. Pain 1998, 77:323-329.
44. Kaufman M.P., Hayes S.G. The exercise pressor reflex. Clin Auton Res 2002, 12:429-439.
45. Kennedy D.S., McNeil C.J., Gandevia S.C. Firing of antagonist small-diameter muscle afferents reduces voluntary activation and torque of elbow flexors. J Physiol 2013, 591:3591-3604.
46. Kennedy D.S., McNeil C.J., Gandevia S.C., Taylor J.L. Fatigue-related firing of distal muscle nociceptors reduces voluntary activation of proximal muscles of the same limb. J Appl Physiol 2014, 116:385-394.
47. Khan M.H., Sinoway L.I. Muscle reflex control of sympathetic nerve activity in heart failure: the role of exercise conditioning. Heart Fail Rev 2000, 5:87-100.
48. Kido K., Gautam M., Benson C.J., Gu H., Brennan T.J. Effect of deep tissue incision on pH responses of afferent fibers and dorsal root ganglia innervating muscle. Anesthesiology 2013, 119:1186-1197.
49. Kindig A.E., Kaufman M.P. Cyclooxygenase blockade attenuates responses of group III and IV muscle afferents to dynamic exercise in cats. Am J Physiol Heart Circ Physiol 2006, 290:H2239-H2246.
50. Kindig A.E., Hayes S.G., Hanna R.L., Kaufman M.P. P2 antagonist PPADS attenuates responses of thin fiber afferents to static contraction and tendon stretch. Am J Physiol Heart Circ Physiol 2006, 290:H1214-H1219.
51. Kniffki K.D., Schomburg E.D., Steffens H. Action of muscular group III and IV afferents on spinal locomotor activity in cat. Brain Res 1980, 186:445-447.
52. Kniffki K.D., Schomburg E.D., Steffens H. Synaptic effects from chemically activated fine muscle afferents upon α-motoneurons in decerebrate and spinal cats. Brain Res 1981, 206:361-370.
53. Kniffki K.D., Schomburg E.D., Steffens H. Effects from fine muscle and cutaneous afferents on spinal locomotion in cats. J Physiol 1981, 319:543-554.
54. Laurin J., Gondin J., Dousset E., Decherchi P. Effect of tenotomy on metabosensitive afferent fibers from tibialis anterior muscle. Exp Brain Res 2008, 186:87-92.
55. Laurin J., Dousset E., Mesure S., Decherchi P. Neuromuscular recovery pattern after medial collateral ligament disruption in rats. J Appl Physiol 2009, 107:98-104.
56. Laurin J., Dousset E., Decherchi P. Modulation of the spinal excitability by muscle metabosensitive afferent fibers. J Neurosci Res 2010, 88:2755-2764.
57. Laurin J., Dousset E., Mesure S., Decherchi P. Neuromuscular recovery after medial collateral ligament disruption and eccentric rehabilitation program. Med Sci Sports Exerc 2011, 43:1032-1041.
58. Le Pera D., Graven-Nielsen T., Valeriani M. Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clin Neurophysiol 2001, 112:1633-1641.
59. Li J., Sinoway A.N., Gao Z., Maile M.D., Pu M., Sinoway L.I. Muscle mechanoreflex and metaboreflex responses after myocardial infarction in rats. Circulation 2004, 110:3049-3054.
60. Light A.R., Hughen R.W., 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 2008, 100:1184-1201.
61. Ling L.J., Honda T., Shimada Y., Ozaki N. Central projection of unmyelinated (C) primary afferent fibers from gastrocnemius muscle in the guinea pig. J Comp Neurol 2003, 461:140-150.
62. Maisky V.A., Pilyavskii A.I., Kalezic I., Ljubisavljevic M., Kostyukov A.I., Windhorst U., Johansson H. NADPH-diaphorase activity and c-fos expression in medullary neurons after fatiguing stimulation of hindlimb muscles in the rat. Auton Neurosci 2002, 101:1-12.
63. Marqueste T., Decherchi P., Desplanches D., Favier R., Grélot L., Jammes Y. Chronic electrostimulation after nerve repair by self-anastomosis: effects on the size, the mechanical, histochemical and biochemical muscle properties. Acta Neuropathol 2006, 111:589-600.
64. Martin P.G., Smith J.L., Butler J.E., Gandevia S.C., Taylor J.L. Fatigue-sensitive afferents inhibit extensor but not flexor motoneurons in humans. J Neurosci 2006, 26:4796-4802.
65. Martin P.G., Weerakkody N., Gandevia S.C. Group III and IV muscle afferents differentially affect the motor cortex and motoneurons in humans. J Physiol 2008, 586:1277-1289.
66. Mense S. Algesic agents exciting muscle nociceptors. Exp Brain Res 2009, 196:89-100.
67. Mense S., Meyer H. Different types of slowly conducting afferent units in cat skeletal muscle and tendon. J Physiol 1985, 363:403-417.
68. Mense S., Stahnke M. Responses in muscle afferent fibres of slow conduction velocity to contractions and ischaemia in the cat. J Physiol 1983, 342:383-397.
69. Michael G.J., Priestley J.V. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci 1999, 19:1844-1854.
70. Middlekauff H.R., Sinoway L.I. Increased mechanoreceptor stimulation explains the exaggerated exercise pressor reflex seen in heart failure. J Appl Physiol 2007, 102:492-496.
71. Middlekauff H.R., Nitzsche E.U., Hoh C.K., Hamilton M.A., Fonarow G.C., Hage A., Moriguchi J.D. Exaggerated muscle mechanoreflex control of reflex renal vasoconstriction in heart failure. J Appl Physiol 2001, 90:1714-1719.
72. Middlekauff H.R., Chiu J., Hamilton M.A., Fonarow G.C., MacLellan W.R., Hage A., Moriguchi J., Patel J. Cyclooxygenase products sensitize muscle mechanoreceptors in humans with heart failure. Am J Physiol Heart Circ Physiol 2008, 294:1956-1962.
73. Mizuno M., Murphy M.N., Mitchell J.H., Smith S.A. Antagonism of the TRPv1 receptor partially corrects muscle metaboreflex overactivity in spontaneously hypertensive rats. J Physiol 2011, 589:6191-6204.
74. Murphy M.N., Mizuno M., Mitchell J.H., Smith S.A. Cardiovascular regulation by skeletal muscle reflexes in health and disease. Am J Physiol Heart Circ Physiol 2011, 301:H1191-H1204.
75. Negrão C.E., Rondon M.U., Tinucci T., Alves M.J., Roveda F., Braga A.M., Reis S.F., Nastari L., Barretto A.C., Krieger E.M., Middlekauff H.R. Abnormal neurovascular control during exercise is linked to heart failure severity. Am J Physiol Heart Circ Physiol 2001, 280:H1286-H1292.
76. Panneton W.M., Gan Q., Juric R. The central termination of sensory fibers from nerves to the gastrocnemius muscle of the rat. Neuroscience 2005, 134:175-187.
77. Pertici V., Amendola J., Laurin J., Gigmes D., Madaschi L., Carelli S., Marqueste T., Gorio A., Decherchi P. The use of poly(N-[2-hydroxypropyl]-methacrylamide) hydrogel to repair a T10 spinal cord hemisection in rat: a behavioural, electrophysiological and anatomical examination. ASN Neuro 2013, 5:149-166.
78. Pettorossi V.E., Torre Della G., Bortolami R., Brunetti O. The role of capsaicin-sensitive muscle afferents in fatigue-induced modulation of the monosynaptic reflex in the rat. J Physiol 1999, 515:599-607.
79. Rojas-Piloni G., Martínez-Lorenzana G., Condés-Lara M., Rodríguez-Jiménez J. Direct sensorimotor corticospinal modulation of dorsal horn neuronal C-fiber responses in the rat. Brain Res 2010, 1351:104-114.
80. Ross J.L., Queme L.F., Shank A.T., Hudgins R.C., Jankowski M.P. Sensitization of group III and IV Muscle Afferents In The Mouse After Ischemia And Reperfusion Injury. J Pain 2014, 20(15):1257-1270.
81. Rossi A., Mazzocchio R., Decchi B. Effect of chemically activated fine muscle afferents on spinal recurrent inhibition in humans. Clin Neurophysiol 2003, 114:279-287.
82. Rotto D.M., Kaufman M.P. Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J Appl Physiol 1988, 64:2306-2313.
83. Rybicki K.J., Waldrop T.G., Kaufman M.P. Increasing gracilis muscle interstitial potassium concentrations stimulate group III and IV afferents. J Appl Physiol 1985, 58:936-941.
84. Schomburg E.D., Steffens H. Only minor spinal motor reflex effects from feline group IV muscle nociceptors. Neurosci Res 2002, 44:213-223.
85. Schomburg E.D., Steffens H.H., Kniffki K.D.K. Contribution of group III and IV muscle afferents to multisensorial spinal motor control in cats. Neurosci Res 1999, 33:195-206.
86. Schomburg E.D., Steffens H., Wada N. Parallel nociceptive reflex pathways with negative and positive feedback functions to foot extensors in the cat. J Physiol 2001, 536:605-613.
87. Schomburg E.D., Steffens H., Maznychenko A.V., Pilyavskii A.I., Hellström F., Kostyukov A.I., Maisky V.A. Acute muscle inflammation enhances the monosynaptic reflexes and c-fos expression in the feline spinal cord. Eur J Pain 2007, 11:579-586.
88. Schomburg E.D., Steffens H., Dibaj P., Sears T.A. Major contribution of Aδ-fibres to increased reflex transmission in the feline spinal cord during acute muscle inflammation. Neurosci Res 2012, 72:155-162.
89. Schomburg E.D., Kalezic I., Dibaj P., Steffens H. Reflex transmission to lumbar α-motoneurons in the mouse similar and different to those in the cat. Neurosci Res 2013, 76:133-140.
90. Simone D., Marchettini P., Caputi G., Ochoa J. Cramping pain and deep hyperalgesia following intramuscular injection of capsaicin. Soc Neurosci Abstr 1992, 18:134.
91. Sluka K.A., O'Donnell J.M., Danielson J., Rasmussen L.A. Regular physical activity prevents development of chronic pain and activation of central neurons. J Appl Physiol (1985) 2013, 15(114):725-733.
92. Smith S.A., Williams M.A., Mitchell J.H., Mammen P.P., Garry M.G. The capsaicin-sensitive afferent neuron in skeletal muscle is abnormal in heart failure. Circulation 2005, 26(111):2056-2065.
93. Smith S.A., Mitchell J.H., Naseem R.H., Garry M.G. Mechanoreflex mediates the exaggerated exercise pressor reflex in heart failure. Circulation 2005, 112:2293-2300.
94. Smith S.A., Downey R.M., Williamson J.W., Mizuno M. Autonomic dysfunction in muscular dystrophy: a theoretical framework for muscle reflex involvement. Front Physiol 2014, 5:47.
95. Stacey M.J. Free nerve endings in skeletal muscle of the cat. J Anat 1969, 105:231-254.
96. Standl T.G., Horn E., Luckmann M., Burmeister M., Wilhelm S., Schulte am Esch J. Subarachnoid sufentanil for early postoperative pain management in orthopedic patients: a placebo-controlled, double-blind study using spinal microcatheters. Anesthesiology 2001, 94:230-238.
97. Taylor J.L., Gandevia S.C. A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 2008, 104:542-550.
98. Taylor J.L., Butler J.E., Gandevia S.C. Changes in muscle afferents, motoneurons and motor drive during muscle fatigue. Eur J Appl Physiol 2000, 83:106-115.
99. Taylor J.L., Allen G.M., Butler J.E., Gandevia S.C. Supraspinal fatigue during intermittent maximal voluntary contractions of the human elbow flexors. J Appl Physiol 2000, 89:305-313.
100. Torre Della G., Lucchi M.L., Brunetti O., Pettorossi V.E. Central projections and entries of capsaicin-sensitive muscle afferents. Brain Res 1996, 713:223-231.
101. Walder R.Y., Gautam M., Wilson S.P., Benson C.J., Sluka K.A. Selective targeting of ASIC3 using artificial miRNAs inhibits primary and secondary hyperalgesia after muscle inflammation. Pain 2011, 152:2348-2356.
102. Wang H.J., Li Y.L., Gao L., Zucker I.H. Alteration in skeletal muscle afferents in rats with chronic heart failure. J Physiol 2010, 588:5033-5047.
103. Wang H.J., Li Y.L., Zucker I.H. Exercise training prevents skeletal muscle afferent sensitization in rats with chronic heart failure. Am J Physiol Regul Integr Comp Physiol 2012, 302:R1260-R1270.
104. Ward N.S. Mechanisms underlying recovery of motor function after stroke. Postgrad Med J 2005, 81:510-514.
105. Williams M.A., Smith S.A., O'Brien D.E., Mitchell J.H., Garry M.G. The group IV afferent neuron expresses multiple receptor alterations in cardiomyopathyic rats: evidence at the cannabinoid CB1 receptor. J Physiol 2008, 586:835-845.
106. Windhorst U., Meyer-Lohmann J., Kirmayer D., Zochodne D. Renshaw cell responses to intra-arterial injection of muscle metabolites into cat calf muscles. Neurosci Res 1997, 27:235-247.
107. Wood J.N., Winter J., James I.F., Rang H.P., Yeats J., Bevan S. Capsaicin-induced ion fluxes in dorsal root ganglion cells in culture. J Neurosci 1988, 8:3208-3220.
108. Zehr E.P. Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 2002, 86:455-468.