New perspectives concerning feedback influences on cardiorespiratory control during rhythmic exercise and on exercise performance

Journal of Physiology

Volumn 590, Issue 17, 2012, Pages 4129-4144

  Dempsey, Jerome A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BREATHING MUSCLE; CARDIOPULMONARY FUNCTION; CAROTID BODY CHEMORECEPTOR; EXERCISE; EXERCISE INTENSITY; FATIGUE; FEEDBACK SYSTEM; HUMAN; HYPERPNEA; LOCOMOTION; MUSCLE BLOOD FLOW; MUSCLE SPINDLE AFFERENT NERVE; NERVE BLOCK; NERVE CELL STIMULATION; NONHUMAN; PHYSICAL PERFORMANCE; PRIORITY JOURNAL; RESPIRATION CONTROL; SENSORY NERVE CONDUCTION; SYMPATHETIC FUNCTION; SYMPATHETIC NERVE;

AFFERENT PATHWAYS; ANIMALS; AWARDS AND PRIZES; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; CAROTID BODY; CHEMORECEPTOR CELLS; EXERCISE; FEEDBACK, PHYSIOLOGICAL; HUMANS; MUSCLE, SKELETAL; PHYSICAL ENDURANCE; PHYSICAL EXERTION; PHYSIOLOGY; RESPIRATORY MUSCLES; RESPIRATORY PHYSIOLOGICAL PHENOMENA;

EID: 84865581165     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.233908     Document Type: Article

References (110)

1. 1-adrenergic constriction than gastrocnemius arterioles. J Appl Physiol 92, 1808-1816.
2. Aaron EA, Johnson BD, Seow CK & Dempsey JA (1992a). Oxygen cost of exercise hyperpnea: measurement. J Appl Physiol 72, 1810-1817.
3. Aaron EA, Seow KC, Johnson BD & Dempsey JA (1992b). Oxygen cost of exercise hyperpnea: implications for performance. J Appl Physiol 72, 1818-1825.
4. Adams L, Frankel H, Garlick J, Guz A, Murphy K & Semple SJ (1984). The role of spinal cord transmission in the ventilatory response to exercise in man. J Physiol 355, 85-97.
5. Adreani CM, Hill JM & Kaufman MP (1997). Responses of group III and IV muscle afferents to dynamic exercise. J Appl Physiol 82, 1811-1817.
6. Alam M & Smirk FH (1937). Observations in man upon a blood pressure raising reflex arising from the voluntary muscles. J Physiol 89, 372-383.
7. Alam M & Smirk FH (1938). Unilateral loss of blood pressure raising, pulse accelerating, reflex from voluntary muscle due to a lesion of the spinal cord. Clin Sci 3, 247-258.
8. Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF & Dempsey JA (2010a). Group III and IV muscle afferents contribute to ventilatory and cardiovascular response to rhythmic exercise in humans. J Appl Physiol 109, 966-976.
9. Amann M, Eldridge MW, Lovering AT, Stickland MK, Pegelow DF & Dempsey JA (2006). Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue in humans. J Physiol 575, 937-952.
10. Amann M, Pegelow DF, Jacques AJ & Dempsey JA (2007). 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.
11. Amann M, Proctor LT, Sebranek JJ, Eldridge MW, Pegelow DF & Dempsey JA (2008). Somatosensory feedback from the limbs exerts inhibitory influences on central neural drive during whole body endurance exercise. J Appl Physiol 105, 1714-1724.
12. Amann M, Proctor LT, Sebranek JJ, Pegelow DF & Dempsey JA (2009). Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 587, 271-283.
13. Amann M, Regan MS, Kobitary M, Eldridge MW, Boutellier U, Pegelow DF & Dempsey JA (2010b). Impact of pulmonary system limitations on locomotor muscle fatigue in patients with COPD. Am J Physiol Regul Integr Comp Physiol 299, R314-R324.
14. Amann M, Runnels S, Morgan DE, Trinity JD, Fjeldstad AS, Wray DW, Reese VR & Richardson RS (2011b). On the contribution of group III and IV muscle afferents to the circulatory response to rhythmic exercise in humans. J Physiol 589, 3855-3866.
15. Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF & Dempsey JA (2011b). Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. J Physiol 589, 5299-5309.
16. Amann M & Secher NH (2010). Point: Afferent feedback from fatigued locomotor muscles is an important determinant of endurance exercise performance. J Appl Physiol 108, 452-454.
17. Andersen P & Saltin B (1985). Maximal perfusion of skeletal muscle in man. J Physiol 366, 233-249.
18. Anholm JD, Johnson RL & Ramanathan M (1987). Changes in cardiac output during sustained maximal ventilation in humans. J Appl Physiol 63, 181-187.
19. Asmussen E, Nielsen M & Wieth-Pedersen G (1943). Cortical or reflex control of respiration during muscular work Acta Physiol Scand 6, 168-175.
20. Babcock MA, Pegelow DF, Harms CA & Dempsey JA (2002). Effects of respiratory muscle unloading on exercise-induced diaphragm fatigue. J Appl Physiol 93, 201-206.
21. Babcock MA, Pegelow DF, McClaran SR, Suman OE & Dempsey JA (1995). Contribution of diaphragmatic power output to exercise-induced diaphragm fatigue. J Appl Physiol 78, 1710-1719.
22. Barclay JK (1986). A delivery-independent blood flow effect on skeletal muscle fatigue. J Appl Physiol 61, 1084-1090.
23. Basnayake SD, Green AL & Paterson DJ (2012). Mapping the central neurocircuitry that integrates the cardiovascular response to exercise in humans. Exp Physiol 97, 29-38.
24. Bisgard GE, Mitchell RA & Herbert DA (1979). Effects of dopamine, norepinephrine and 5-hydroxytryptamine on the carotid body of the dog. Respir Physiol 37, 61-80.
25. 2. J Physiol 588, 2455-2471.
26. Calbet JA, Gonzalez-Alonso J, Helge JW, Sondergaard H, Munch-Andersen T, Boushel R & Saltin B (2007). Cardiac output and leg and arm blood flow during incremental exercise to exhaustion on the cycle ergometer. J Appl Physiol 103, 969-978.
27. Coote JH, Hilton SM & Perez-Gonzalez JF (1971). The reflex nature of the pressor response to muscular exercise. J Physiol 215, 789-804.
28. 2 sensitivity. PLoS Med 4, e239.
29. Degtyarenko AM & Kaufman MP (2002). Spinoreticular neurons that receive group III input are inhibited by MLR stimulation. J Appl Physiol 93, 92-98.
30. Dejours P, Mithoefer JC & Raynaud J (1957). Evidence against the existence of specific ventilatory chemoreceptors in the legs. J Appl Physiol 10, 367-371.
31. Dempsey JA, Romer L, Rodman J, Miller J & Smith C (2006). Consequences of exercise-induced respiratory muscle work. Respir Physiol Neurobiol 151, 242-250.
32. Derchak PA, Sheel AW, Morgan BJ & Dempsey JA (2002). Effects of expiratory muscle work on muscle sympathetic nerve activity. J Appl Physiol 92, 1539-1552.
33. Ding Y, Li YL & Schultz HD (2011). Role of blood flow in carotid body chemoreflex function in heart failure. J Physiol 589, 245-258.
34. Duron B (1981). Intercostal and diaphragmatic muscle endings and afferents. In Regulation of Breathing, pp. 473-540. Dekker, New York.
35. Eiken O (1987). Responses to dynamic leg exercise in man as influenced by changes in muscle perfusion pressure. Acta Physiol Scand Suppl 566, 1-37.
36. Eldridge FL, Millhorn DE & Waldrop TG (1981). Exercise hyperpnea and locomotion: parallel activation from the hypothalamus. Science 211, 844-846.
37. Fernandes A, Galbo H, Kjaer M, Mitchell JH, Secher NH & Thomas SN (1990). Cardiovascular and ventilatory responses to dynamic exercise during epidural anaesthesia in man. J Physiol 420, 281-293.
38. Fink GR, Adams L, Watson JD, Innes JA, Wuyam B, Kobayashi I, Corfield DR, Murphy K, Jones T, Frackowiak RS & Guz A (1995). Hyperpnoea during and immediately after exercise in man: evidence of motor cortical involvement. J Physiol 489, 663-675.
39. Forster HV, Haouzi P & Dempsey JA (2012). Control of breathing during exercise. Compr Physiol 2, 743-777.
40. Freund PR, Rowell LB, Murphy TM, Hobbs SF & Butler SH (1979). Blockade of the pressor response to muscle ischemia by sensory nerve block in man. Am J Physiol Heart Circ Physiol 237, H433-H439.
41. Gagnon P, Bussieres JS, Ribeiro F, Gagnon SL, Saey D, Gagne N, Provencher S & Maltais F (2012). Influences of Spinal Anesthesia on Exercise Tolerance in Patients with COPD. Am J Respir Crit Care Med (ePub).
42. Galbo H, Kjaer M & Secher NH (1987). Cardiovascular, ventilatory and catecholamine responses to maximal dynamic exercise in partially curarized man. J Physiol 389, 557-568.
43. Gandevia SC (2001). Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81, 1725-1789.
44. Gandevia SC, Allen GM, Butler JE & Taylor JL (1996). Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol 490, 529-536.
45. Garland SJ & Kaufman MP (1995). Role of muscle afferents in the inhibition of motoneurons during fatigue. Adv Exp Med Biol 384, 271-278.
46. Green AL, Wang S, Purvis S, Owen SL, Bain PG, Stein JF, Guz A, Aziz TZ & Paterson DJ (2007). Identifying cardiorespiratory neurocircuitry involved in central command during exercise in humans. J Physiol 578, 605-612.
47. Haouzi P, Chenuel B & Huszczuk A (2004). Sensing vascular distension in skeletal muscle by slow conducting afferent fibers: neurophysiological basis and implication for respiratory control. J Appl Physiol 96, 407-418.
48. Haouzi P, Hill JM, Lewis BK & Kaufman MP (1999). Responses of group III and IV muscle afferents to distension of the peripheral vascular bed. J Appl Physiol 87, 545-553.
49. Harms CA, Babcock MA, McClaran SR, Pegelow DF, Nickele GA, Nelson WB & Dempsey JA (1997). Respiratory muscle work compromises leg blood flow during maximal exercise. J Appl Physiol 82, 1573-1583.
50. Harms CA, Wetter TJ, McClaran SR, Pegelow DF, Nickele GA, Nelson WB, Hanson P & Dempsey JA (1998). Effects of respiratory muscle work on cardiac output and its distribution during maximal exercise. J Appl Physiol 85, 609-618.
51. Harms CA, Wetter TJ, St Croix CM, Pegelow DF & Dempsey JA (2000). Effects of respiratory muscle work on exercise performance. J Appl Physiol 89, 131-138.
52. Hayes SG, Kindig AE & Kaufman MP (2006). Cyclooxygenase blockade attenuates responses of group III and IV muscle afferents to dynamic exercise in cats. Am J Physiol Heart Circ Physiol 290, H2239-H2246.
53. Hill JM (2000). Discharge of group IV phrenic afferent fibers increases during diaphragmatic fatigue. Brain Res 856, 240-244.
54. Hill JM & Kaufman MP (1990). Attenuation of reflex pressor and ventilatory responses to static muscular contraction by intrathecal opioids. J Appl Physiol 68, 2466-2472.
55. 31P-MRS study. J Appl Physiol 86, 1367-1373.
56. Hornbein TF, Sorensen SC & Parks CR (1969). Role of muscle spindles in lower extremities in breathing during bicycle exercise. J Appl Physiol 27, 476-479.
57. Hussain SN, Chatillon A, Comtois A, Roussos C & Magder S (1991). Chemical activation of thin-fibre phrenic afferents. 2. Cardiovascular responses. J Appl Physiol 70, 77-86.
58. Jammes Y & Balzamo E (1992). Changes in afferent and efferent phrenic activities with electrically induced diaphragmatic fatigue. J Appl Physiol 73, 894-902.
59. Kaufman MP (2010). Control of breathing during dynamic exercise by thin fibre muscle afferents. J Appl Physiol 109, 947-948.
60. Kaufman MP (2012). The exercise pressor reflex in animals. Exp Physiol 97, 51-58.
61. Kjaer M, Hanel B, Worm L, Perko G, Lewis SF, Sahlin K, Galbo H & Secher NH (1999). Cardiovascular and neuroendocrine responses to exercise in hypoxia during impaired neural feedback from muscle. Am J Physiol Regul Integr Comp Physiol 277, R76-R85.
62. Light AR, Hughen RW, Zhang J, Rainier J, Liu Z & Lee J (2008). 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.
63. McCloskey DI & Mitchell JH (1972). Reflex cardiovascular and respiratory responses originating in exercising muscle. J Physiol 224, 173-186.
64. McConnell AK & Lomax M (2006). The influence of inspiratory muscle work history and specific inspiratory muscle training upon human limb muscle fatigue. J Physiol 577, 445-457.
65. Maltais F, LeBlanc P, Whittom F, Simard C, Marquis K, Belanger M, Breton MJ & Jobin J (2000). Oxidative enzyme activities of the vastus lateralis muscle and the functional status in patients with COPD. Thorax 55, 848-853.
66. Manohar M (1986). Blood flow to the respiratory and limb muscles and to abdominal organs during maximal exertion in ponies. J Physiol 377, 25-35.
67. Marcora S (2010). Counterpoint: Afferent feedback from fatigued locomotor muscles is not an important determinant of endurance exercise performance. J Appl Physiol 108, 454-456.
68. Meintjes AF, Nobrega AC, Fuchs IE, Ally A & Wilson LB (1995). Attenuation of the exercise pressor reflex. Effect of opioid agonist on substance P release in L-7 dorsal horn of cats. Circ Res 77, 326-334.
69. Miller JD, Smith CA, Hemauer SJ & Dempsey JA (2007). The effects of inspiratory intrathoracic pressure production on the cardiovascular response to submaximal exercise in health and chronic heart failure. Am J Physiol Heart Circ Physiol 292, H580-H592.
70. Mitchell JH, Reeves DR Jr, Rogers HB & Secher NH (1989). Epidural anaesthesia and cardiovascular responses to static exercise in man. J Physiol 417, 13-24.
71. Morin D & Viala D (2002). Coordinations of locomotor and respiratory rhythms in vitro are critically dependent on hindlimb sensory inputs. J Neurosci 22, 4756-4765.
72. Musch TI (1993). Elevated diaphragmatic blood flow during submaximal exercise in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 265, H1721-H1726.
73. Nielsen AM, Bisgard GE & Vidruk EH (1988). Carotid chemoreceptor activity during acute and sustained hypoxia in goats. J Appl Physiol 65, 1796-1802.
74. Olson TP, Joyner MJ, Dietz NM, Eisenach JH, Curry TB & Johnson BD (2010). Effects of respiratory muscle work on blood flow distribution during exercise in heart failure. J Physiol 588, 2487-2501.
75. Pickar JG, Hill JM & Kaufman MP (1994). Dynamic exercise stimulates group III muscle afferents. J Neurophysiol 71, 753-760.
76. Plowey ED, Kramer JM, Beatty JA & Waldrop TG (2002). In vivo electrophysiological responses of pedunculopontine neurons to static muscle contraction. Am J Physiol Regul Integr Comp Physiol 283, R1008-R1019.
77. Pomeroy G, Ardell JL & Wurster RD (1986). Spinal opiate modulation of cardiovascular reflexes in the exercising dog. Brain Res 381, 385-389.
78. Road JD (1990). Phrenic afferents and ventilatory control. Lung 168, 137-149.
79. Rodman JR, Henderson KS, Smith CA & Dempsey JA (2003). Cardiovascular effects of the respiratory muscle metaboreflexes in dogs: rest and exercise. J Appl Physiol 95, 1159-1169.
80. Romer LM, Lovering AT, Haverkamp HC, Pegelow DF & Dempsey JA (2006). Effect of inspiratory muscle work on peripheral fatigue of locomotor muscles in healthy humans. J Physiol 571, 425-439.
81. Romer LM, McConnell AK & Jones DA (2002). Effects of inspiratory muscle training on time-trial performance in trained cyclists. J Sports Sci 20, 547-562.
82. Rowell LB (2004). Ideas about control of skeletal and cardiac muscle blood flow (1876-2003): cycles of revision and new vision. J Appl Physiol 97, 384-392.
83. Rowell LB, Hermansen L & Blackmon JR (1976). Human cardiovascular and respiratory responses to graded muscle ischemia. J Appl Physiol 41, 693-701.
84. Rowell LB & O'Leary DS (1990). Reflex control of the circulation during exercise: chemoreflexes and mechanoreflexes. J Appl Physiol 69, 407-418.
85. St Croix CM, Morgan BJ, Wetter TJ & Dempsey JA (2000). Fatiguing inspiratory muscle work causes reflex sympathetic activation in humans. J Physiol 529, 493-504.
86. Schultz HD (2011). Angiotensin and carotid body chemoreception in heart failure. Curr Opin Pharmacol 11, 144-149.
87. Seals DR, Johnson DG & Fregosi RF (1991). Hypoxia potentiates exercise-induced sympathetic neural activation in humans. J Appl Physiol 71, 1032-1040.
88. Sheel AW, Derchak PA, Morgan BJ, Pegelow DF, Jacques AJ & Dempsey JA (2001). Fatiguing inspiratory muscle work causes reflex reduction in resting leg blood flow in humans. J Physiol 537, 277-289.
89. Sheel AW, Derchak PA, Pegelow DF & Dempsey JA (2002). Threshold effects of respiratory muscle work on limb vascular resistance. Am J Physiol Heart Circ Physiol 282, H1732-H1738.
90. Smith SA, Querry RG, Fadel PJ, Gallagher KM, Stromstad M, Ide K, Raven PB & Secher NH (2003). Partial blockade of skeletal muscle somatosensory afferents attenuates baroreflex resetting during exercise in humans. J Physiol 551, 1013-1021.
91. Starling EH (1920). On the circulatory changes associated with exercise. J Royal Army Med Corps 34, 258-272.
92. Stickland MK, Fuhr DP, Haykowsky MJ, Jones KE, Paterson DI, Ezekowitz JA & McMurtry MS (2011). Carotid chemoreceptor modulation of blood flow during exercise in healthy humans. J Physiol 589, 6219-6230.
93. Stickland MK, Miller JD, Smith CA & Dempsey JA (2007). Carotid chemoreceptor modulation of regional blood flow distribution during exercise in health and chronic heart failure. Circ Res 100, 1371-1378.
94. Stickland MK, Morgan BJ & Dempsey JA (2008). Carotid chemoreceptor modulation of sympathetic vasoconstrictor outflow during exercise in healthy humans. J Physiol 586, 1743-1754.
95. Strange S, Secher NH, Pawelczyk JA, Karpakka J, Christensen NJ, Mitchell JH & Saltin B (1993). Neural control of cardiovascular responses and of ventilation during dynamic exercise in man. J Physiol 470, 693-704.
96. Sun SY, Wang W, Zucker IH & Schultz HD (1999). Enhanced activity of carotid body chemoreceptors in rabbits with heart failure: role of nitric oxide. J Appl Physiol 86, 1273-1282.
97. Taylor JL & Gandevia SC (2008). A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104, 542-550.
98. Teppema LJ & Dahan A (2010). The ventilatory response to hypoxia in mammals: mechanisms, measurement, and analysis. Physiol Rev 90, 675-754.
99. Thornton JM, Guz A, Murphy K, Griffith AR, Pedersen DL, Kardos A, Leff A, Adams L, Casadei B & Paterson DJ (2001). Identification of higher brain centres that may encode the cardiorespiratory response to exercise in humans. J Physiol 533, 823-836.
100. Tibes U (1977). Reflex inputs to the cardiovascular and respiratory centers from dynamically working canine muscles. Some evidence for involvement of group III or IV nerve fibers. Circ Res 41, 332-341.
101. Verges S, Lenherr O, Haner AC, Schulz C & Spengler CM (2007). Increased fatigue resistance of respiratory muscles during exercise after respiratory muscle endurance training. Am J Physiol Regul Integr Comp Physiol 292, R1246-R1253.
102. Vissing J, MacLean DA, Vissing SF, Sander M, Saltin B & Haller RG (2001). The exercise metaboreflex is maintained in the absence of muscle acidosis: insights from muscle microdialysis in humans with McArdle's disease. J Physiol 537, 641-649.
103. Vogiatzis I, Athanasopoulos D, Boushel R, Guenette JA, Koskolou M, Vasilopoulou M, Wagner H, Roussos C, Wagner PD & Zakynthinos S (2008). Contribution of respiratory muscle blood flow to exercise-induced diaphragmatic fatigue in trained cyclists. J Physiol 586, 5575-5587.
104. Vogiatzis I, Athanasopoulos D, Habazettl H, Kuebler WM, Wagner H, Roussos C, Wagner PD & Zakynthinos S (2009). Intercostal muscle blood flow limitation in athletes during maximal exercise. J Physiol 587, 3665-3677.
105. Waldrop TG & Iwamoto GA (2006). Point: Supraspinal locomotor centers do contribute significantly to the hyperpnea of dynamic exercise. J Appl Physiol 100, 1077-1079.
106. Waldrop TG, Mullins DC & Millhorn DE (1986). Control of respiration by the hypothalamus and by feedback from contracting muscles in cats. Respir Physiol 64, 317-328.
107. Wang ZY, Olson EB Jr, Bjorling DE, Mitchell GS & Bisgard GE (2008). Sustained hypoxia-induced proliferation of carotid body type I cells in rats. J Appl Physiol 104, 803-808.
108. Weil JV, Byrne-Quinn E, Sodal IE, Kline JS, McCullough RE & Filley GF (1972). Augmentation of chemosensitivity during mild exercise in normal man. J Appl Physiol 33, 813-819.
109. Wetter TJ, Harms CA, Nelson WB, Pegelow DF & Dempsey JA (1999). Influence of respiratory muscle work on and leg blood flow during submaximal exercise. J Appl Physiol 87, 643-651.
110. Witt JD, Guenette JA, Rupert JL, McKenzie DC & Sheel AW (2007). Inspiratory muscle training attenuates the human respiratory muscle metaboreflex. J Physiol 584, 1019-1028.