Muscle reflex in heart failure: The role of exercise training

Frontiers in Physiology

Volumn 3 OCT, Issue , 2012, Pages

  Wang, Han Jun ^a   Zucker, Irving H ^a   Wang, Wei ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Exercise; Muscle afferents; Myocardial infarction; Physical training; Sympathetic nerve activity

Indexed keywords

EID: 84870894033     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00398     Document Type: Article

References (123)

1. Adreani, C. M., Hill, J. M., and Kaufman, M. P. (1997). Responses of group III and IV muscle afferents to dynamic exercise. J. Appl. Physiol. 82, 1811-1817.
2. Adreani, C. M., and Kaufman, M. P. (1998). Effect of arterial occlusion on responses of group III and IV afferents to dynamic exercise. J. Appl. Physiol. 84, 1827-1833.
3. Alam, M., and Smirk, F. H. (1937). Observations in man upon a blood pressure raising reflex arising from the voluntary muscles. J. Physiol. 89, 372-383.
4. Andres, K. H., von Düring, M., and Schmidt, R. F. (1985). Sensory innervation of the Achilles tendon by group III and IV afferent fibers. Anat. Embryol. (Berl.) 172, 145-156.
5. Batista, M. L. Jr., Rosa, J. C., Lopes, R. D., Lira, F. S., Martins, E. Jr., Yamashita, A. S., et al. (2010). Exercise training changes IL-10/TNF-alpha ratio in the skeletal muscle of post-MI rats. Cytokine 49, 102-108.
6. Belardinelli, R., Georgiou, D., Cianci, G., and Purcaro, A. (1999). Randomized, controlled trial of long-term moderate exercise training in chronic heart failure: effects on functional capacity, quality of life, and clinical outcome. Circulation 99, 1173-1182.
7. Chen, C. C., England, S., Akopian, A. N., and Wood, J. N. (1998). A sensory neuron-specific, proton-gated ion channel. Proc. Natl. Acad. Sci. U.S.A. 95, 10240-10245.
8. Cohn, J. N. (1990). Abnormalities of peripheral sympathetic nervous system control in congestive heart failure. Circulation 82, I59-I67.
9. Costa, F., and Biaggioni, I. (1994). Role of adenosine in the sympathetic activation produced by isometric exercise in humans. J. Clin. Invest. 93, 1654-1660.
10. Crayton, S. C., Mitchell, J. H., and Payne, F. C. III. (1981). Reflex cardiovascular response during injection of capsaicin into skeletal muscle. Am. J. Physiol. 240, H315-H319.
11. De Matos, L. D., Gardenghi, G., Rondon, M. U., Soufen, H. N., Tirone, A. P., Barretto, A. C., et al. (2004). Impact of 6 months of therapy with carvedilol on muscle sympathetic nerve activity in heart failure patients. J. Card. Fail. 10, 496-502.
12. Drexler, H., Riede, U., Munzel, T., Konig, H., Funke, E., and Just, H. (1992). Alterations of skeletal muscle in chronic heart failure. Circulation 85, 1751-1759.
13. Dykes, R. W., and Craig, A. D. (1998). Control of size and excitability of mechanosensory receptive fields in dorsal column nuclei by homolateral dorsal horn neurons. J. Neurophysiol. 80, 120-129.
14. Eldridge, F. L., Millhorn, D. E., Kiley, J. P., and Waldrop, T. G. (1985). Stimulation by central command of locomotion, respiration and circulation during exercise. Respir. Physiol. 59, 313-337.
15. Fisher, W. J., and White, M. J. (1999). Training-induced adaptations in the central command and peripheral reflex components of the pressor response to isometric exercise of the human triceps surae. J. Physiol. 520(Pt 2), 621-628.
16. Fletcher, G. F., Balady, G., Blair, S. N., Blumenthal, J., Caspersen, C., Chaitman, B., et al. (1996). Statement on exercise: benefits and recommendations for physical activity programs for all Americans. A statement for health professionals by the Committee on Exercise and Cardiac Rehabilitation of the Council on Clinical Cardiology, American Heart Association. Circulation 94, 857-862.
17. Fletcher, G. F., Balady, G. J., Amsterdam, E. A., Chaitman, B., Eckel, R., Fleg, J., et al. (2001). Exercise standards for testing and training: a statement for healthcare professionals from the American Heart Association. Circulation 104, 1694-1740.
18. Flynn, K. E., Pina, I. L., Whellan, D. J., Lin, L., Blumenthal, J. A., Ellis, S. J., et al. (2009). Effects of exercise training on health status in patients with chronic heart failure: HF-ACTION randomized controlled trial. JAMA 301, 1451-1459.
19. Franciosa, J. A., Park, M., and Levine, T. B. (1981). Lack of correlation between exercise capacity and indexes of resting left ventricular performance in heart failure. Am. J. Cardiol. 47, 33-39.
20. Francis, G. S. (1985). Neurohumoral mechanisms involved in congestive heart failure. Am. J. Cardiol. 55, 15A-21A.
21. Gao, L., Wang, W., Liu, D., and Zucker, I. H. (2007). Exercise training normalizes sympathetic outflow by central antioxidant mechanisms in rabbits with pacing-induced chronic heart failure. Circulation 115, 3095-3102.
22. Garry, M. G. (2011). Abnormalities of the exercise pressor reflex in heart failure. Exerc. Sport Sci. Rev. 39, 167-176.
23. Goodwin, G. M., McCloskey, D. I., and Mitchell, J. H. (1972). Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension. J. Physiol. 226, 173-190.
24. Grassi, G., and Mancia, G. (1999). Sympathetic overactivity and exercise intolerance in heart failure: a cause-effect relationship. Eur. Heart J. 20, 854-855.
25. Guenther, S., Reeh, P. W., and Kress, M. (1999). Rises in [Ca2+]i mediate capsaicin- and proton-induced heat sensitization of rat primary noci-ceptive neurons. Eur. J. Neurosci. 11, 3143-3150.
26. Halbert, J. A., Silagy, C. A., Finucane, P., Withers, R. T., Hamdorf, P. A., and Andrews, G. R. (1997). The effectiveness of exercise training in lowering blood pressure: a meta-analysis of randomised controlled trials of 4 weeks or longer. J. Hum. Hypertens. 11, 641-649.
27. Hambrecht, R., Fiehn, E., Yu, J., Niebauer, J., Weigl, C., Hilbrich, L., et al. (1997). Effects of endurance training on mitochondrial ultra-structure and fiber type distribution in skeletal muscle of patients with stable chronic heart failure. J. Am. Coll. Cardiol. 29, 1067-1073.
28. Hanna, R. L., and Kaufman, M. P. (2003). Role played by purinergic receptors on muscle afferents in evoking the exercise pressor reflex. J. Appl. Physiol. 94, 1437-1445.
29. Hanna, R. L., and Kaufman, M. P. (2004). Activation of thin-fiber muscle afferents by a P2X agonist in cats. J. Appl. Physiol. 96, 1166-1169.
30. Hayward, L., Wesselmann, U., and Rymer, W. Z. (1991). Effects of muscle fatigue on mechanically sensitive afferents of slow conduction velocity in the cat triceps surae. J. Neurophysiol. 65, 360-370.
31. Hellsten, Y., Maclean, D., Radegran, G., Saltin, B., and Bangsbo, J. (1998). Adenosine concentrations in the interstitium of resting and contracting human skeletal muscle. Circulation 98, 6-8.
32. Howald, H., Hoppeler, H., Claassen, H., Mathieu, O., and Straub, R. (1985). Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflugers Arch. 403, 369-376.
33. Iwamoto, G. A., and Botterman, B. R. (1985). Peripheral factors influencing expression of pressor reflex evoked by muscular contraction. J. Appl. Physiol. 58, 1676-1682.
34. Iwamoto, G. A., Botterman, B. R., and Waldrop, T. G. (1984). The exercise pressor reflex: evidence for an afferent pressor pathway outside the dor-solateral sulcus region. Brain Res. 292, 160-164.
35. Iwamoto, G. A., and Kaufman, M. P. (1987). Caudal ventrolateral medullary cells responsive to muscular contraction. J. Appl. Physiol. 62, 149-157.
36. Iwamoto, G. A., Kaufmann, M. P., Botterman, B. R., and Mitchell, J. H. (1982). Effects of lateral reticu-lar nucleus lesions on the exercise pressor reflex in cats. Circ. Res. 51, 400-403.
37. Iwamoto, G. A., Waldrop, T. G., Kaufman, M. P., Botterman, B. R., Rybicki, K. J., and Mitchell, J. H. (1985). Pressor reflex evoked by muscular contraction: contributions by neuraxis levels. J. Appl. Physiol. 59, 459-467.
38. Jankowska, E. A., Wegrzynowska, K., Superlak, M., Nowakowska, K., Lazorczyk, M., Biel, B., et al. (2007). The 12-week progressive quadriceps resistance training improves muscle strength, exercise capacity and quality of life in patients with stable chronic heart failure. Int. J. Cardiol. 130, 36-43.
39. Jordt, S. E., Tominaga, M., and Julius, D. (2000). Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc. Natl. Acad. Sci. U.S.A. 97, 8134-8139.
40. Kalia, M., Mei, S. S., and Kao, F. F. (1981). Central projections from ergoreceptors (C fibers) in muscle involved in cardiopulmonary responses to static exercise. Circ. Res. 48, I48-I62.
41. Kaufman, M. P., Iwamoto, G. A., Longhurst, J. C., and Mitchell, J. H. (1982). Effects of capsaicin and bradykinin on afferent fibers with ending in skeletal muscle. Circ. Res. 50, 133-139.
42. Kaufman, M. P., Longhurst, J. C., Rybicki, K. J., Wallach, J. H., and Mitchell, J. H. (1983). Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. J. Appl. Physiol. 55, 105-112.
43. Kaufman, M. P., Rybicki, K. J., Waldrop, T. G., and Ordway, G. A. (1984). Effect of ischemia on responses of group III and IV afferents to contraction. J. Appl. Physiol. 57, 644-650.
44. Khan, M. H., and Sinoway, L. I. (2000). Muscle reflex control of sympathetic nerve activity in heart failure: the role of exercise conditioning. Heart Fail. Rev. 5, 87-100.
45. Kindig, A. E., Hayes, S. G., Hanna, R. L., and Kaufman, M. P. (2006). P2 antagonist PPADS attenuates responses of thin fiber afferents to static contraction and tendon stretch. Am. J. Physiol. Heart Circ. Physiol. 290, H1214-H1219.
46. Kindig, A. E., Heller, T. B., and Kaufman, M. P. (2005). VR-1 receptor blockade attenuates the pres-sor response to capsaicin but has no effect on the pressor response to contraction in cats. Am. J. Physiol. Heart Circ. Physiol. 288, H1867-H1873.
47. Kniffki, K. D., Mense, S., and Schmidt, R. F. (1978). Responses of group IV afferent units from skeletal muscle to stretch, contraction and chemical stimulation. Exp. Brain Res. 31, 511-522.
48. Koba, S., Gao, Z., and Sinoway, L. I. (2009). Oxidative stress and the muscle reflex in heart failure. J. Physiol. 587, 5227-5237.
49. Koba, S., Xing, J., Sinoway, L. I., and Li, J. (2008). Sympathetic nerve responses to muscle contraction and stretch in ischemic heart failure. Am. J. Physiol. Heart Circ. Physiol. 294, H311-H321.
50. Koba, S., Yoshida, T., and Hayashi, N. (2006). Differential sympathetic outflow and vasoconstriction responses at kidney and skeletal muscles during fictive locomotion. Am. J. Physiol. Heart Circ. Physiol. 290, H861-H868.
51. Kozelka, J. W., and Wurster, R. D. (1985). Ascending spinal pathways for somatoautonomic reflexes in the anesthetized dog. J. Appl. Physiol. 58, 1832-1839.
52. Li, J., Hand, G. A., Potts, J. T., Wilson, L. B., and Mitchell, J. H. (1997). c-Fos expression in the medulla induced by static muscle contraction in cats. Am. J. Physiol. 272, H48-H56.
53. Li, J., King, N. C., and Sinoway, L. I. (2003). ATP concentrations and muscle tension increase linearly with muscle contraction. J. Appl. Physiol. 95, 577-583.
54. Li, J., King, N. C., and Sinoway, L. I. (2005). Interstitial ATP and nore-pinephrine concentrations in active muscle. Circulation 111, 2748-2751.
55. Li, J., and Mitchell, J. H. (2000). c-Fos expression in the midbrain peri-aqueductal gray during static muscle contraction. Am. J. Physiol. Heart Circ. Physiol. 279, H2986-H2993.
56. Li, J., and Mitchell, J. H. (2002). Role of NO in modulating neuronal activity in superficial dorsal horn of spinal cord during exercise pressor reflex. Am. J. Physiol. Heart Circ. Physiol. 283, H1012-H1018.
57. Li, J., Sinoway, A. N., Gao, Z., Maile, M. D., Pu, M., and Sinoway, L. I. (2004). Muscle mechanoreflex and meta-boreflex responses after myocardial infarction in rats. Circulation 110, 3049-3054.
58. Linke, A., Adams, V., Schulze, P. C., Erbs, S., Gielen, S., Fiehn, E., et al. (2005). Antioxidative effects of exercise training in patients with chronic heart failure: increase in radical scavenger enzyme activity in skeletal muscle. Circulation 111, 1763-1770.
59. Liu, J. L., Irvine, S., Reid, I. A., Patel, K. P., and Zucker, I. H. (2000). Chronic exercise reduces sympathetic nerve activity in rabbits with pacing-induced heart failure: a role for angiotensin II. Circulation 102, 1854-1862.
60. Longhurst, J. C., and Mitchell, J. H. (1979). Reflex control of the circulation by afferents from skeletal muscle. Int. Rev. Physiol. 18, 125-148.
61. Mancini, D. M., Walter, G., Reichek, N., Lenkinski, R., McCully, K. K., Mullen, J. L., et al. (1992). Contribution of skeletal muscle atrophy to exercise intolerance and altered muscle metabolism in heart failure. Circulation 85, 1364-1373.
62. McClain, J., Hardy, C., Enders, B., Smith, M., and Sinoway, L. (1993). Limb congestion and sympathoexcitation during exercise. Implications for congestive heart failure. J. Clin. Invest. 92, 2353-2359.
63. McCloskey, D. I., and Mitchell, J. H. (1972). Reflex cardiovascular and respiratory responses originating in exercising muscle. J. Physiol. 224, 173-186.
64. McCord, J. L., Tsuchimochi, H., and Kaufman, M. P. (2009). Acid-sensing ion channels contribute to the metaboreceptor component of the exercise pressor reflex. Am. J. Physiol. Heart Circ. Physiol. 297, H443-H449.
65. McCord, J. L., Tsuchimochi, H., Yamauchi, K., Leal, A., and Kaufman, M. P. (2011). Tempol attenuates the exercise pressor reflex independently of neutralizing reactive oxygen species in femoral artery ligated rats. J. Appl. Physiol. 111, 971-979.
66. Mense, S., and Craig, A. D. Jr. (1988). Spinal and supraspinal terminations of primary afferent fibers from the gastrocnemius-soleus muscle in the cat. Neuroscience 26, 1023-1035.
67. Mense, S., and Meyer, H. (1985). Different types of slowly conducting afferent units in cat skeletal muscle and tendon. J. Physiol. 363, 403-417.
68. Michael, G. J., and Priestley, J. V. (1999). Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregu-lation by axotomy. J. Neurosci. 19, 1844-1854.
69. Middlekauff, H. R., and Chiu, J. (2004). Cyclooxygenase products sensitize muscle mechanorecep-tors in healthy humans. Am. J. Physiol. Heart Circ. Physiol. 287, H1944-H1949.
70. Middlekauff, H. R., Chiu, J., Hamilton, M. A., Fonarow, G. C., Maclellan, W. R., Hage, A., et al. (2004). Muscle mechanoreceptor sensitivity in heart failure. Am. J. Physiol. Heart Circ. Physiol. 287, H1937-H1943.
71. Middlekauff, H. R., Nitzsche, E. U., Hoh, C. K., Hamilton, M. A., Fonarow, G. C., Hage, A., et al. (2000). Exaggerated renal vasocon-striction during exercise in heart failure patients. Circulation 101, 784-789.
72. Middlekauff, H. R., Nitzsche, E. U., Hoh, C. K., Hamilton, M. A., Fonarow, G. C., Hage, A., et al. (2001). Exaggerated muscle mechanoreflex control of reflex renal vasoconstriction in heart failure. J. Appl. Physiol. 90, 1714-1719.
73. Mostoufi-Moab, S., Herr, M. D., Silber, D. H., Gray, K. S., Leuenberger, U. A., and Sinoway, L. I. (2000). Limb congestion enhances the synchronization of sympathetic outflow with muscle contraction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R478-R483.
74. Mostoufi-Moab, S., Widmaier, E. J., Cornett, J. A., Gray, K., and Sinoway, L. I. (1998). Forearm training reduces the exercise pressor reflex during ischemic rhythmic handgrip. J. Appl. Physiol. 84, 277-283.
75. Mueller, P. J. (2007a). Exercise training and sympathetic nervous system activity: evidence for physical activity dependent neural plasticity. Clin. Exp. Pharmacol. Physiol. 34, 377-384.
76. Mueller, P. J. (2007b). Exercise training attenuates increases in lumbar sympathetic nerve activity produced by stimulation of the rostral ventrolat-eral medulla. J. Appl. Physiol. 102, 803-813.
77. Mueller, P. J., and Hasser, E. M. (2006). Putative role of the NTS in alterations in neural control of the circulation following exercise training in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R383-R392.
78. Murata, J., and Matsukawa, K. (2001). Cardiac vagal and sympathetic efferent discharges are differentially modified by stretch of skeletal muscle. Am. J. Physiol. Heart Circ. Physiol. 280, H237-H245.
79. Murphy, M. N., Mizuno, M., Mitchell, J. H., and Smith, S. A. (2011). Cardiovascular regulation by skeletal muscle reflexes in health and disease. Am. J. Physiol. Heart Circ. Physiol. 301, H1191-H1204.
80. Myers, J., Dziekan, G., Goebbels, U., and Dubach, P. (1999). Influence of high-intensity exercise training on the ventilatory response to exercise in patients with reduced ventricular function. Med. Sci. Sports Exerc. 31, 929-937.
81. Myers, J., and Froelicher, V. F. (1991). Hemodynamic determinants of exercise capacity in chronic heart failure. Ann. Intern. Med. 115, 377-386.
82. Negrao, C. E., and Middlekauff, H. R. (2008). Adaptations in autonomic function during exercise training in heart failure. Heart Fail. Rev. 13, 51-60.
83. O'Connor, C. M., Whellan, D. J., Lee, K. L., Keteyian, S. J., Cooper, L. S., Ellis, S. J., et al. (2009). Efficacy and safety of exercise training in patients with chronic heart failure: HF-ACTION randomized controlled trial. JAMA 301, 1439-1450.
84. Piepoli, M., Clark, A. L., Volterrani, M., Adamopoulos, S., Sleight, P., and Coats, A. J. (1996). Contribution of muscle afferents to the hemo-dynamic, autonomic, and ventila-tory responses to exercise in patients with chronic heart failure: effects of physical training. Circulation 93, 940-952.
85. Piepoli, M., Ponikowski, P., Clark, A. L., Banasiak, W., Capucci, A., and Coats, A. J. (1999). A neural link to explain the "muscle hypothesis" of exercise intolerance in chronic heart failure. Am. Heart J. 137, 1050-1056.
86. Piepoli, M. F. (2006). Exercise training in heart failure. Curr. Heart Fail. Rep. 3, 189-196.
87. Piepoli, M. F., and Coats, A. J. (2007). Increased metaboreceptor stimulation explains the exaggerated exercise pressor reflex seen in heart failure. J. Appl. Physiol. 102, 494-496.
88. Piepoli, M. F., Davos, C., Francis, D. P., and Coats, A. J. (2004). Exercise training meta-analysis of trials in patients with chronic heart failure (ExTraMATCH). BMJ 328, 189.
89. Piepoli, M. F., Dimopoulos, K., Concu, A., and Crisafulli, A. (2008). Cardiovascular and ventilatory control during exercise in chronic heart failure: role of muscle reflexes. Int. J. Cardiol. 130, 3-7.
90. Pina, I. L., Apstein, C. S., Balady, G. J., Belardinelli, R., Chaitman, B. R., Duscha, B. D., et al. (2003). Exercise and heart failure: a statement from the American Heart Association Committee on exercise, rehabilitation, and prevention. Circulation 107, 1210-1225.
91. Pliquett, R. U., Cornish, K. G., Patel, K. P., Schultz, H. D., Peuler, J. D., and Zucker, I. H. (2003). Amelioration of depressed cardiopulmonary reflex control of sympathetic nerve activity by short-term exercise training in male rabbits with heart failure. J. Appl. Physiol. 95, 1883-1888.
92. Rondon, E., Brasileiro-Santos, M. S., Moreira, E. D., Rondon, M. U., Mattos, K. C., Coelho, M. A., et al. (2006). Exercise training improves aortic depressor nerve sensitivity in rats with ischemia-induced heart failure. Am. J. Physiol. Heart Circ. Physiol. 291, H2801-H2806.
93. Roveda, F., Middlekauff, H. R., Rondon, M. U., Reis, S. F., Souza, M., Nastari, L., et al. (2003). The effects of exercise training on sympathetic neural activation in advanced heart failure: a randomized controlled trial. J. Am. Coll. Cardiol. 42, 854-860.
94. Sinoway, L., Shenberger, J., Leaman, G., Zelis, R., Gray, K., Baily, R., et al. (1996). Forearm training attenuates sympathetic responses to prolonged rhythmic forearm exercise. J. Appl. Physiol. 81, 1778-1784.
95. Sinoway, L. I., and Li, J. (2005). A perspective on the muscle reflex: implications for congestive heart failure. J. Appl. Physiol. 99, 5-22.
96. Smart, N., and Marwick, T. H. (2004). Exercise training for patients with heart failure: a systematic review of factors that improve mortality and morbidity. Am. J. Med. 116, 693-706.
97. Smith, S. A., Leal, A. K., Williams, M. A., Murphy, M. N., Mitchell, J. H., and Garry, M. G. (2010). The TRPv1 receptor is a mediator of the exercise pressor reflex in rats. J. Physiol. 588, 1179-1189.
98. Smith, S. A., Mammen, P. P., Mitchell, J. H., and Garry, M. G. (2003). Role of the exercise pressor reflex in rats with dilated cardiomyopathy. Circulation 108, 1126-1132.
99. Smith, S. A., Mitchell, J. H., and Garry, M. G. (2006a). The mammalian exercise pressor reflex in health and disease. Exp. Physiol. 91, 89-102.
100. Smith, S. A., Williams, M. A., Leal, A. K., Mitchell, J. H., and Garry, M. G. (2006b). Exercise pressor reflex function is altered in spontaneously hypertensive rats. J. Physiol. 577, 1009-1020.
101. Smith, S. A., Mitchell, J. H., Naseem, R. H., and Garry, M. G. (2005a). Mechanoreflex mediates the exaggerated exercise pressor reflex in heart failure. Circulation 112, 2293-2300.
102. Smith, S. A., Williams, M. A., Mitchell, J. H., Mammen, P. P., and Garry, M. G. (2005b). The capsaicin-sensitive afferent neuron in skeletal muscle is abnormal in heart failure. Circulation 111, 2056-2065.
103. Sterns, D. A., Ettinger, S. M., Gray, K. S., Whisler, S. K., Mosher, T. J., Smith, M. B., et al. (1991). Skeletal muscle metaboreceptor exercise responses are attenuated in heart failure. Circulation 84, 2034-2039.
104. Sullivan, M. J., Green, H. J., and Cobb, F. R. (1990). Skeletal muscle biochemistry and histology in ambulatory patients with long-term heart failure. Circulation 81, 518-527.
105. Sullivan, M. J., and Hawthorne, M. H. (1995). Exercise intolerance in patients with chronic heart failure. Prog. Cardiovasc. Dis. 38, 1-22.
106. Thomas, G. D., and Segal, S. S. (2004). Neural control of muscle blood flow during exercise. J. Appl. Physiol. 97, 731-738.
107. Thomas, G. D., Zhang, W., and Victor, R. G. (2001). Impaired modulation of sympathetic vasoconstric-tion in contracting skeletal muscle of rats with chronic myocardial infarctions: role of oxidative stress. Circ. Res. 88, 816-823.
108. Tominaga, M., Caterina, M. J., Malmberg, A. B., Rosen, T. A., Gilbert, H., Skinner, K., et al. (1998). The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21, 531-543.
109. Vulchanova, L., Arvidsson, U., Riedl, M., Wang, J., Buell, G., Surprenant, A., et al. (1996). Differential distribution of two ATP-gated channels (P2X receptors) determined by immunocytochemistry. Proc. Natl. Acad. Sci. U.S.A. 93, 8063-8067.
110. Vulchanova, L., Riedl, M. S., Shuster, S. J., Buell, G., Surprenant, A., North, R. A., et al. (1997). Immunohistochemical study of the P2X2 and P2X3 receptor sub-units in rat and monkey sensory neurons and their central terminals. Neuropharmacology 36, 1229-1242.
111. Vulchanova, L., Riedl, M. S., Shuster, S. J., Stone, L. S., Hargreaves, K. M., Buell, G., et al. (1998). P2X3 is expressed by DRG neurons that terminate in inner lamina II. Eur. J. Neurosci. 10, 3470-3478.
112. Waldrop, T. G., and Mitchell, J. H. (1985). Effects of barodenervation on cardiovascular responses to static muscular contraction. Am. J. Physiol. 249, H710-H714.
113. Wang, H. J., Li, Y. L., Gao, L., Zucker, I. H., and Wang, W. (2010a). Alteration in skeletal muscle affer-ents in rats with chronic heart failure. J. Physiol. 588, 5033-5047.
114. Wang, H. J., Pan, Y. X., Wang, W. Z., Gao, L., Zimmerman, M. C., Zucker, I. H., et al. (2010b). Exercise training prevents the exaggerated exercise pressor reflex in rats with chronic heart failure. J. Appl. Physiol. 108, 1365-1375.
115. Wang, H. J., Li, Y. L., Zhang, L. B., Zucker, I. H., Gao, L., Zimmerman, M. C., et al. (2011). Endogenous reactive oxygen species modulates voltage-gated sodium channels in dorsal root ganglia of rats. J. Appl. Physiol. 110, 1439-1447.
116. Wang, H. J., Li, Y. L., Zucker, I. H., and Wang, W. (2012). Exercise training prevents skeletal muscle afferent sensitization in rats with chronic heart failure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 320, R1260-R1270.
117. Wang, H. J., Pan, Y. X., Wang, W. Z., Zucker, I. H., and Wang, W. (2009). NADPH oxidase-derived reactive oxygen species in skeletal muscle modulates the exercise pressor reflex. J. Appl. Physiol. 107, 450-459.
118. Welch, J. M., Simon, S. A., and Reinhart, P. H. (2000). The activation mechanism of rat vanilloid receptor 1 by capsaicin involves the pore domain and differs from the activation by either acid or heat. Proc. Natl. Acad. Sci. U.S.A. 97, 13889-13894.
119. Wilson, J. R. (1995). Exercise intolerance in heart failure. Importance of skeletal muscle. Circulation 91, 559-561.
120. Wilson, L. B., Andrew, D., and Craig, A. D. (2002). Activation of spinobul-bar lamina I neurons by static muscle contraction. J. Neurophysiol. 87, 1641-1645.
121. Wilson, L. B., Dyke, C. K., Parsons, D., Wall, P. T., Pawelczyk, J. A., Williams, R. S., et al. (1995). Effect of skeletal muscle fiber type on the pressor response evoked by static contraction in rabbits. J. Appl. Physiol. 79, 1744-1752.
122. Wisloff, U., Stoylen, A., Loennechen, J. P., Bruvold, M., Rognmo, O., Haram, P. M., et al. (2007). Superior cardiovascular effect of aerobic interval training versus moderate continuous training in heart failure patients: a randomized study. Circulation 115, 3086-3094.
123. Zhang, P., and Canessa, C. M. (2001). Single-channel properties of recom-binant acid-sensitive ion channels formed by the subunits ASIC2 and ASIC3 from dorsal root ganglion neurons expressed in Xenopus oocytes. J. Gen. Physiol. 117, 563-572.