Muscle sympathetic activity in resting and exercising humans with and without heart failure

Applied Physiology, Nutrition and Metabolism

Volumn 40, Issue 11, 2015, Pages 1107-1115

  Notarius, Catherine F ^a   Millar, Philip J ^b   Floras, John S ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

Exercise; Exercise training; Heart failure; HFrEF; Microneurography; Muscle sympathetic nerve activity; Peak oxygen uptake

Indexed keywords

ACTION POTENTIAL; ADRENERGIC SYSTEM; EXERCISE; EXERCISE TOLERANCE; HEART FAILURE; HUMAN; INNERVATION; MUSCLE CONTRACTION; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; REFLEX; REST; SKELETAL MUSCLE;

ACTION POTENTIALS; EXERCISE; EXERCISE TOLERANCE; HEART FAILURE; HUMANS; MUSCLE CONTRACTION; MUSCLE, SKELETAL; OXYGEN CONSUMPTION; REFLEX; REST; SYMPATHETIC NERVOUS SYSTEM;

EID: 84945894722     PISSN: 17155312     EISSN: 17155320     Source Type: Journal    
DOI: 10.1139/apnm-2015-0289     Document Type: Review

References (104)

1. Abboud, F., and Kumar, R. 2014. Obstructive sleep apnea and insight into mechanisms of sympathetic overactivity. J. Clin. Invest. 124: 1454–1457. doi:10.1172/JCI70420. PMID:24691480.
2. Alvarez, G.E., Halliwill, J.R., Ballard, T.P., Beske, S.D., and Davy, K.P. 2005. Sympathetic neural regulation in endurance-trained humans: fitness vs fatness. J. Appl. Physiol. 98: 498–502. PMID:15489260.
3. Alves, M.J., Rondon, M.U., Santos, A.C., Dias, R.G., Barretto, A.C., Krieger, E.M., et al. 2007. Sympathetic nerve activity restrains reflex vasodilation in heart failure. Clin. Auton. Res. 17: 364–369. doi:10.1007/s10286-007-0448-6. PMID:18043866.
4. Alves, M.J.N.N., dos Santos, M.R., Nobre, T.S., Martinez, D.G., Barretto, A.C.P., Brum, P.C., et al. 2012. Mechanisms of blunted muscle vasodilation during peripheral chemoreceptor stimulation in heart failure patients. Hypertension, 60: 669–676. doi:10.1161/HYPERTENSIONAHA.112.195776. PMID:22802226.
5. Andersen, P., Adams, R.P., Sjoqaard, G., Thorboe, A., and Saltin, B. 1985. Dynamic knee extension as model for study of isolated exercising muscle in humans. J. Appl. Physiol. 59: 1647–1653. PMID:4066596.
6. Ando, S., Dajani, H.R., and Floras, J.S. 1997a. Frequency domain characteristics of muscle sympathetic nerve activity in heart failure and healthy humans. Am. J. Physiol. 273: R205–R212. PMID:9249551.
7. Ando, S., Dajani, H.R., Senn, B.L., Newton, G.E., and Floras, J.S. 1997b. Sympathetic alternans. Evidence for arterial baroreflex control of muscle sympathetic nerve activity in congestive heart failure. Circulation, 95: 316–319. PMID:9008442.
8. Antunes-Correa, L.M., Melo, R.C., Nobre, T.S., Ueno, L.M., Franco, F.G., Braga, A.M.W., et al. 2010. Impact of gender on benefits of exercise training on sympathetic nerve activity and muscle blood flow in heart failure. Eur. J. Heart Fail. 12: 58–65. doi:10.1093/eurjhf/hfp168. PMID:20023046.
9. Antunes-Correa, L.M., Kanamura, B.Y., Melo, R.C., Nobre, T.S., Ueno, L.M., Franco, F.G., et al. 2012. Exercise training improves neurovascular control and functional capacity in heart failure patients regardless of age. Eur. J. Prev. Cardiol. 19: 822–829. doi:10.1177/1741826711414626. PMID:21697210.
10. Azevedo, E.R., Newton, G.E., and Parker, J.D. 1999. Cardiac and systemic sympathetic activity in response to clonidine in human heart failure. J. Am. Coll. Cardiol. 33: 186–191. doi:10.1016/S0735-1097(98)00524-5. PMID:9935028.
11. Azevedo, E.R., Newton, G.E., Floras, J.S., and Parker, J.D. 2000. Reducing cardiac filling pressure lowers norepinephrine spillover in patients with chronic heart failure. Circulation, 101: 2053–2059. doi:10.1161/01.CIR.101.17.2053.
12. Barretto, A.C.P., Santos, A.C., Munhoz, R., Rondon, M.U.P.B., Franco, F.G., Trombetta, I.C., et al. 2009. Increased muscle sympathetic nerve activity predicts mortality in heart failure patients. Int. J. Cardiol. 135: 302–307. doi:10.1016/j.ijcard.2008.03.056. PMID:18582965.
13. Batman, B.A., Hardy, J.C., Leuenberger, U.A., Smith, M.B., Yang, Q.X., and Sinoway, L.I. 1994. Sympathetic nerve activity during prolonged rhythmic forearm exercise. J. Appl. Physiol. 76: 1077–1081. PMID:8005848.
14. Carter, J.R., and Ray, C.A. 2015. Sympathetic neural adaptations to exercise training in humans. Auton. Neurosci. Basic Clin. 188: 36–43. PMID:25458425.
15. Carter, J.R., Ray, C.A., Downs, E.M., and Cooke, W.H. 2003. Strength training reduces arterial blood pressure but not sympathetic neural activity in young normotensive subjects. J. Appl. Physiol. 94: 2212–2216. PMID:12562680.
16. Charkoudian, N., Joyner, M.J., Sokolnicki, L.A., Johnson, C.P., Eisenach, J.H., Dietz, N.M., et al. 2006. Vascular adrenergic responsiveness is inversely related to tonic activity of sympathetic vasoconstrictor nerves in humans. J. Physiol. 572(3): 821–827. doi:10.1113/jphysiol.2005.104075. PMID:16513672.
17. Cohn, J.N., Levine, T.B., Olivari, M.T., Garberg, V., Lura, D., Francis, G.S., et al. 1984. Plasma norepinephrine as a guide to prognosis in patients with chronic congestive heart failure. N. Engl. J. Med. 311: 819–823. doi:10.1056/NEJM198409273111303. PMID:6382011.
18. Cohn, J.N., Johnson, G.R., Shabetai, R., Loeb, H., Tristani, F., Rector, T., et al. 1993. Ejection fraction, peak exercise oxygen consumption, cardiothoracic ratio, ventricular arrhythmias, and plasma norepinephrine as determinants of prognosis in heart failure. The V-HeFT VA Cooperative Studies Group. Circulation, 87: VI5–V16.PMID:8500240.
19. Crisafulli, A., Salis, E., Tocco, F., Melis, F., Milia, R., Pittau, G., et al. 2007. Impaired central hemodynamic response and exaggerated vasoconstriction during muscle metaboreflex activation in heart failure patients. Am. J. Physiol. 292: H2988–H2996. PMID:17308012.
20. Despas, F., Lambert, E., Vaccaro, A., Labrunee, M., Franchitto, N., Lebrun, M., et al. 2012. Peripheral chemoreflex activation contributes to sympathetic baroreflex impairment in chronic heart failure. J. Hypertens. 30: 753–760. PMID:22241144.
21. Dibner-Dunlap, M.E., Smith, M.L., Kinugawa, T., and Thames, M.D. 1996. Enalaprilat augments arterial and cardiopulmonary baroreflex control of sympathetic nerve activity in patients with heart failure. J. Am. Coll. Cardiol. 27: 358–364. doi:10.1016/0735-1097(95)00484-X. PMID:8557906.
22. Dinenno, F.A., Jones, P.P., Seals, D.R., and Tanaka, H. 1999. Limb blood flow and vascular conductance are reduced with age in healthy humans: relation to elevations in sympathetic nerve activity and declines in oxygen demand. Circulation, 100: 164–170. doi:10.1161/01.CIR.100.2.164.
23. Esler, M., Jennings, G.L., Korner, P., Willett, I., Dudley, F., Hasking, G.J., et al. 1988. Assessment of human sympathetic nervous system activity from measurements of norepinephrine turnover. Hypertension, 11: 3–20. doi:10.1161/01.HYP.11.1.3. PMID:2828236.
24. Esposito, F., Mathieu-Costello, O., Shabetai, R., Wagner, P.D., and Richardson, R.S. 2010. Limited maximal exercise capacity in patients with chronic heart failure: partitioning the contributors. J. Am. Coll. Cardiol. 55: 1945–1954. doi:10.1016/j.jacc.2009.11.086. PMID:20430267.
25. Ferguson, D.W., Berg, W.J., and Sanders, J.S. 1990. Clinical and hemodynamic correlates of sympathetic nerve activity in normal humans and patients with heart failure: evidence from direct microneurographic recordings. J. Am. Coll. Cardiol. 16: 1125–1134. doi:10.1016/0735-1097(90)90544-Y. PMID:2229759.
26. Floras, J.S. 2001. Arterial baroreceptor and cardiopulmonary reflex control of sympathetic outflow in human heart failure. Ann. N.Y. Acad. Sci. 940: 500–513. PMID:11458705.
27. Floras, J.S. 2009. Sympathetic nervous system activation in human heart failure: clinical implications of an updated model. J. Am. Coll. Cardiol. 54: 375–385. doi:10.1016/j.jacc.2009.03.061. PMID:19628111.
28. Floras, J.S., and Hara, K. 1993. Sympathoneural and haemodynamic characteristics of young subjects with mild essential hypertension. J. Hypertens. 11: 647–655. doi:10.1097/00004872-199306000-00009. PMID:8397244.
29. Floras, J.S., and Ponikowski, P. 2015. The sympathetic/parasympathetic imbalance in heart failure with reduced ejection fraction. Eur. Heart J. 36: 1974–1982. doi:10.1093/eurheartj/ehv087.
30. Floras, J.S., Jones, J.V., Hassan, M.O., Osikowska, B.A., Sever, P.S., and Sleight, P. 1986. Failure of plasma norepinephrine to consistently reflect sympathetic activity in humans. Hypertension, 8: 641–649. doi:10.1161/01.HYP.8.8.641.
31. Floras, J.S., Sinkey, C.A., Aylward, P.E., Seals, D.R., Thoren, P.N., and Mark, A.L. 1989. Postexercise hypotension and sympathoinhibition in borderline hypertensive men. Hypertension, 14: 28–35. doi:10.1161/01.HYP.14.1.28.
32. Forster, C., and Armstrong, P.W. 1990. Pacing-induced heart failure in the dog: evaluation of peripheral vascular α-adrenoceptor subtypes. J. Cardiovasc. Pharmacol. 16: 708–718. doi:10.1097/00005344-199011000-00004.
33. Forster, C., Carter, S., and Armstrong, P. 1989. Vascular smooth muscle responsiveness to noradrenaline and phenylephrine following experimental heart failure in dogs. Cardiovasc. Res. 23: 489–497. doi:10.1093/cvr/23.6.489. PMID:2590922.
34. Fraga, R., Franco, F.G., Roveda, F., de Matos, L.N., Braga, A.M.W., Rondon, M.U.P.B., et al. 2007. Exercise training reduces sympathetic nerve activity in heart failure patients treated with carvedilol. Eur. J. Heart Fail. 9: 630–636. doi:10.1016/j.ejheart.2007.03.003.
35. 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. doi:10.1016/0002-9149(81)90286-1.
36. Grassi, G., and Esler, M. 1999. How to assess sympathetic activity in humans. J. Hypertens. 17: 719–734. doi:10.1097/00004872-199917060-00001.
37. Grassi, G., Bolla, G., Quarti-Trevano, F., Arenare, F., Brambilla, G., and Mancia, G. 2008. Sympathetic activation in congestive heart failure: reproducibility of neuroadrenergic markers. Eur. J. Heart Fail. 10: 1186–1191. doi:10.1016/j.ejheart.2008.09.013.
38. Grassi, G., Seravalle, G., Brambilla, G., Buzzi, S., Volpe, M., Cesana, F., et al. 2014. Regional differences in sympathetic activation in lean and obese normotensive individuals with obstructive sleep apnoea. J. Hypertens. 32: 383–388. doi:10.1097/HJH.0000000000000034.
39. Hammond, R.L., Augustyniak, R.A., Rossi, N.F., Churchill, P.C., Lapanowsky, K., and O’Leary, D.S. 2000. Heart failure alters the strength and mechanisms of the muscle metaboreflex. Am. J. Physiol. 278: H818–H828. PMID:10710350.
40. Hansen, J., Thomas, G.D., Jacobsen, T.N., and Victor, R.G. 1994. Muscle metaboreflex triggers parallel sympathetic activation in exercising and resting human skeletal muscle. Am. J. Physiol. 266: H2508–H2514. PMID:8024012.
41. Hara, K., and Floras, J.S. 1996. After-effects of exercise on haemodynamics and sympathetic nerve activity in young subjects with dilated cardiomyopathy. Heart, 75: 602–608. doi:10.1136/hrt.75.6.602.
42. Hart, E.C., Charkoudian, N., Wallin, B.G., Curry, T.B., Eisenach, J.H., and Joyner, M.J. 2009. Sex differences in sympathetic neural-hemodynamic balance: implications for human blood pressure regulation. Hypertension, 53: 571–576. doi:10.1161/HYPERTENSIONAHA.108.126391.
43. Hasking, G.J., Esler, M.D., Jennings, G.L., Burton, D., Johns, J.A., and Korner, P.I. 1986. Norepinephrine spillover to plasma in patients with congestive heart failure: evidence of increased overall and cardiorenal sympathetic nervous activity. Circ. 73: 615–621. doi:10.1161/01.CIR.73.4.615.
44. Hasking, G.J., Esler, M.D., Jennings, G.L., Dewar, E., and Lambert, G. 1988. Norepinephrine spillover to plasma during steady-state supine bicycle exercise: comparison of patients with congestive heart failure and normal subjects. Circulation, 78: 516–521. doi:10.1161/01.CIR.78.3.516.
45. Ichinose, M., Saito, M., Fujii, N., Ogawa, T., Hayashi, K., Kondo, N., and Nishiyasu, T. 2008. Modulation of the control of muscle sympathetic nerve activity during incremental leg cycling. J. Physiol. 586: 2753–2766. doi:10.1113/jphysiol.2007.150060.
46. Jensen, E.W., Espersen, K., Kanstrup, I.L., and Christensen, N.J. 1994. Exerciseinduced changes in plasma catecholamines and neuropeptide Y: relation to age and sampling times. J. Appl. Physiol. 76: 1269–1273. PMID:8005872.
47. Katayama, K., Ishida, K., Iwamoto, E., Iemitsu, M., Koike, T., and Saito, M. 2011. Hypoxia auments muscle sympathetic neural response to leg cycling. Am. J. Physiol. 301: R456–R464. PMID:21593431.
48. Kaye, D.M., Lefkovits, J., Jennings, G.L., Bergin, P., Broughton, A., and Esler, M.D. 1995. Adverse consequences of high sympathetic nerve activity in the failing human heart. J. Am. Coll. Cardiol. 26: 1257–1263. doi:10.1016/0735-1097(95)00332-0.
49. Kingwell, B.A., Thompson, J.M., McPherson, G.A., Kaye, D.M., Jennings, G.L., and Esler, M.D. 1995. Comparison of heart rate spectral analysis with cardiac noradrenaline spillover and muscle sympathetic nerve activity in human subjects. In Computer Analysis of Cardiovascular Signals. Edited by M. Di Rienzo, G. Mancia, G. Parati, A. Pedotti, and A. Zanchetti. IOS Press, Amsterdam, Netherlands. pp. 167–176.
50. Kuniyoshi, R.R., Matinelli, M., Negrao, C.E., Siqueira, S.F., Rondon, M.U., Trombetta, I.C., et al. 2014. Effects of cardiac resynchronization therapy on muscle sympathetic nerve activity. Pacing Clin. Electrophysiol. 37: 11–18. doi:10.1111/pace.12254.
51. Lang, C.C., Rayos, G.H., Chomsky, D.B., Wood, A.J.J., and Wilson, J.R. 1997. Effect of sympathoinhibition on exercise performance in patients with heart failure. Circulation, 96: 238–245. doi:10.1161/01.CIR.96.1.238.
52. Leimbach, W.N., Wallin, B.G., Victor, R.G., Aylward, P.E., Sundlof, G., and Mark, A.L. 1986. Direct evidence from intraneural recordings for increased central sympathetic outflow in patients with heart failure. Circulation, 73:913–919. doi:10.1161/01.CIR.73.5.913.
53. Mark, A.L., Victor, R.G., Nerhed, C., and Wallin, B.G. 1985. Microneurographic studies of the mechanisms of sympathetic nerve responses to static exercise in humans. Circ. Res. 57: 461–469. doi:10.1161/01.RES.57.3.461.
54. Middlekauff, H.R., and Sinoway, L.I. 2007. Point:Counterpoint: Increased mechanoreceptor/ metaboreceptor stimulation explains the exaggerated exercise pressor reflex seen in heart failure. J. Appl. Physiol. 102: 492–494. doi:10.1152/japplphysiol.00994.2006.
55. 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. 287: H1937–H1943. PMID:15475527.
56. Millar, P.J., Murai, H., Morris, B.L., and Floras, J.S. 2013. Microneurographic evidence in middle-aged healthy humans for a sympathoexcitatory reflex activated by atrial pressure. Am. J. Physiol. 305: H931–H938. PMID:23851279.
57. Millar, P.J., Murai, H., and Floras, J.S. 2015. Paradoxical muscle sympathetic reflex activation in human heart failure. Circulation, 131: 459–468. doi:10.1161/CIRCULATIONAHA.114.010765.
58. Mitchell, J.H. 1990. J.B. Wolffe memorial lecture. Neural control of the circulation during exercise. Med. Sci. Sports Exerc. 22: 141–154. PMID:2192221.
59. Moreau, K.I., Donato, A.J., Tanaka, H., Jones, P.P., Gates, P.E., and Seals, D.R. 2003. Basal leg blood flow in healthy women is related to age and hormone replacement therapy status. J. Physiol. 547: 309–316. doi:10.1113/jphysiol.2002.032524.
60. Murai, H., Takamura, M., Maruyama, M., Nakano, M., Ikeda, T., Kobayashi, D., et al. 2009. Altered firing pattern of single-unit muscle sympathetic nerve activity during handgrip exercise in chronic heart failure. J. Physiol. 587:2613–2622. doi:10.1113/jphysiol.2009.172627.
61. Ng, A.V., Callister, R., Johnson, D.G., and Seals, D.R. 1993. Age and gender influence muscle sympathetic nerve activity at rest in healthy humans. Hypertension, 21: 498–503. doi:10.1161/01.HYP.21.4.498.
62. Notarius, C.F., and Floras, J.S. 2007. Increased mechanoreceptor/metaboreceptor stimulation explains the exaggerated exercise pressor reflex seen in heart failure. J. Appl. Physiol. 102: 824. doi:10.1152/japplphysiol.01330.2006.
63. Notarius, C.F., Ando, S., Rongen, G.A., and Floras, J.S. 1999a. Resting muscle sympathetic nerve activity and peak oxygen uptake in heart failure and normal subjects. Eur. Heart J. 20: 880–887. doi:10.1053/euhj.1998.1447.
64. Notarius, C.F., Butler, G.C., Ando, S., Pollard, M.J., Senn, B., and Floras, J.S. 1999b. Dissociation between microneurographic and heart rate variability estimates of sympathetic tone in normal subjects and patients with heart failure. Clin. Sci. 96: 557–565. doi:10.1042/cs0960557. PMID:10334961.
65. Notarius, C.F., Atchison, D.J., and Floras, J.S. 2001. Impact of heart failure and exercise capacity on sympathetic response to handgrip exercise. Am. J. Physiol. 280: H969–H976. PMID:11179037.
66. Notarius, C.F., Azevedo, E.R., Parker, J.D., and Floras, J.S. 2002. Peak oxygen uptake is not determined by cardiac noradrenaline spillover in heart failure. Eur. Heart J. 23: 800–805. doi:10.1053/euhj.2001.2942.
67. Notarius, C.F., Spaak, J., Morris, B.L., and Floras, J.S. 2007. Comparison of muscle sympathetic activity in ischemic and nonischemic heart failure. J. Cardiac Fail. 13: 470–475. doi:10.1016/j.cardfail.2007.03.014.
68. Notarius, C.F., Morris, B.L., and Floras, J.S. 2009. Dissociation between reflex sympathetic and forearm vascular responses to lower body negative pressure in heart failure patients with coronary artery disease. Am. J. Physiol. 297: H1760–H1766. PMID:19734366.
69. Notarius, C.F., Murai, H., Morris, B.L., and Floras, J.S. 2012. Effect of fitness on reflex sympathetic neurovascular transduction in middle-age men. Med. Sci. Sports Exerc. 44: 232–237. doi:10.1249/MSS.0b013e31822a68a5. PMID:21701410.
70. Notarius, C.F., Millar, P.J., Murai, H., Morris, B.L., and Floras, J.S. 2014. Inverse relationship between muscle sympathetic activity during exercise and peak oxygen uptake in subjects with and without heart failure. J. Am. Coll. Cardiol. 63: 605–606. doi:10.1016/j.jacc.2013.08.693.
71. Notarius, C.F., Millar, P.J., Murai, H., Morris, B.L., Marzolini, S., Oh, P., and Floras, J.S. 2015. Divergent muscle sympathetic responses to dynamic leg exercise in heart failure and age-matched healthy subjects. J. Physiol. 593: 715–722. doi:10.1113/jphysiol.2014.281873.
72. Petersson, M., Friberg, P., Eisenhofer, G., Lambert, G., and Rundqvist, B. 2005. Long-term outcome in relation to renal sympathetic activity in patients with chronic heart failure. Eur. Heart J. 26: 906–913. doi:10.1093/eurheartj/ehi184.
73. Piepoli, M.F., and Coats, A.J.S. 2007. Counterpoint: Increased metaboreceptor stimulation explains the exaggerated exercise pressor reflex seen in heart failure. J. Appl. Physiol. 102: 494–496. doi:10.1152/japplphysiol.00994a.2006.
74. 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. Circ. 107: 1210–1225. doi:10.1161/01.CIR.0000055013.92097.40.
75. Ray, C.A. 1999. Sympathetic adaptations to one-legged training. J. Appl. Physiol. 86: 1583–1587. PMID:10233121.
76. Ray, C.A., and Carrasco, D. 2000. Isometric handgrip training reduces arterial pressure at rest without changes in sympathetic activity. Am. J. Physiol. 279: H245–H249. PMID:10899063.
77. Ray, C.A., Rea, R.F., Clary, M.P., and Mark, A.L. 1993. Muscle sympathetic nerve responses to dynamic one-legged exercise: effect of body posture. Am. J. Physiol. 264: H1–H7. PMID:8430836.
78. Rea, R.F., and Wallin, B.G. 1989. Sympathetic nerve activity in arm and leg muscles during lower body negative pressure in humans. J. Appl. Physiol. 66: 2778–2781. PMID:2745341.
79. Roveda, F., Middlekauff, H.R., Urbana, M., Rondon, P.B., Reis, S.F., Souza, M., et al. 2003. The effects of exercise training on sympathetic neural activation in advanced heart failure. J. Am. Coll. Cardiol. 42: 854–860. doi:10.1016/S0735-1097(03)00831-3.
80. Rundqvist, B., Elam, M., Bergmann-Sverrisdottir, Y., Eisenhofer, G., and Friberg, P. 1997. Increased cardiac adrenergic drive precedes generalized sympathetic activation in human heart failure. Circulation, 95: 169–175. doi:10.1161/01.CIR.95.1.169.
81. Saito, M., and Mano, T. 1991. Exercise mode affects muscle sympathetic nerve responsiveness. Jpn. J. Physiol. 41: 143–151. doi:10.2170/jjphysiol.41.143.
82. Saito, M., Tsukanaka, A., Yanagihara, D., and Mano, T. 1993. Muscle sympathetic nerve responses to graded leg cycling. J. Appl. Physiol. 75: 663–667. PMID:8226466.
83. Saito, M., Iwase, S., and Hachiya, T. 2009. Resistance exercise training enhances sympathetic nerve activity during fatigue-inducing isometric handgrip trials. Eur. J. Appl. Physiol. 105: 225–234. doi:10.1007/s00421-008-0893-5.
84. Santos, A.C., Alves, M.J.N.N., Rondon, M.U.P.B., Barretto, A.C.P., Middlekauff, H.R., and Negrao, C.E. 2005. Sympathetic activation restrains endothelium-mediated muscle vasodilation in heart failure patients. Am. J. Physiol. 289: H593–H599. PMID:15778282.
85. Schultz, H.D., Li, Y.L., and Ding, Y. 2007. Arterial chemoreceptors and sympathetic nerve activity: implications for hypertension and heart failure. Hypertension, 50: 6–13. doi:10.1161/HYPERTENSIONAHA.106.076083.
86. Seals, D.R. 1991. Sympathetic neural adjustments to stress in physically trained and untrained humans. Hypertension, 17: 36–43. doi:10.1161/01.HYP.17.1.36.
87. Seals, D.R., and Esler, M.D. 2000. Human ageing and the sympathoadrenal system. J. Physiol. 528: 407–417. doi:10.1111/j.1469-7793.2000.00407.x.
88. Sheldahl, L.M., Ebert, T.J., Cox, B., and Tristani, F.E. 1994. Effect of aerobic training on baroreflex regulation of cardiac and sympathetic function. J. Appl. Physiol. 76: 158–165.
89. Silber, D.H., Sutliff, G., Yang, Q.X., Smith, M.B., Sinoway, L.I., and Leuenberger, U. 1998. Altered mechanisms of sympathetic activation during rhythmic forearm exercise in heart failure. J. Appl. Physiol. 84: 1551–1559. PMID:9572798.
90. Sinoway, L.I., Rea, R.F., Mosher, T.J., Smith, M.B., and Mark, A.L. 1992. Hydrogen ion concentration is not the sole determinant of muscle metaboreceptor responses in humans. J. Clin. Invest. 89: 1875–1884. doi:10.1172/JCI115792.
91. Sinoway, L.I., Shenberger, J., Leaman, G., Zelis, R., Gray, K., Baily, R., and Leuenberger, U. 1996. Forearm training attenuates sympathetic responses to prolonged rhythmic forearm exercise. J. Appl. Physiol. 81: 1778–1784. PMID:8904599.
92. Soares-Miranda, L., Franco, F.G., Roveda, F., Martinez, D.G., Rondon, M.U.P.B., Mota, J., et al. 2011. Effects of exercise training on neurovascular responses during handgrip exercise in heart failure patients. Int. J. Cardiol. 146: 122–125. doi:10.1016/j.ijcard.2010.09.091.
93. Somers, V.K., Leo, K.C., Shields, R., Clary, M., and Mark, A.L. 1992. Forearm endurance training attenuates sympathetic nerve response to isometric handgrip in normal humans. J. Appl. Physiol. 72: 1039–1043. PMID:1568957.
94. Spaak, J., Egri, Z.J., Kubo, T., Yu, E., Ando, S., Kaneko, Y., et al. 2005. Muscle sympathetic nerve activity during wakefulness in heart failure patients with and without sleep apnea. Hypertension, 46: 1327–1332. doi:10.1161/01.HYP.0000193497.45200.66.
95. Stelken, A.M., Younis, L.T., Jennison, S.H., Miller, D.D., Miller, L.W., Shaw, L.J., et al. 1996. Prognostic value of cardiopulmonary exercise testing using percent achieved of predicted peak oxygen uptake for patients with ischemic and dilated cardiomyopathy. J. Am. Coll. Cardiol. 27: 345–352. PMID:8557904.
96. Sterns, D.A., Ettinger, S.E., Gray, K.S., Whisler, S.K., Mosher, T.J., Smith, M.B., and Sinoway, L.I. 1991. Skeletal muscle metaboreceptor exercise responses are attenuated in heart failure. Circulation, 84: 2034–2039. doi:10.1161/01.CIR.84.5.2034.
97. Stickland, M.K., Morgan, B.J., and Dempsey, J.A. 2008. Carotid chemoreceptor modulation of sympathetic vasoconstrictor outflow during exercise in healthy humans. J. Physiol. 586: 1743–1754. doi:10.1113/jphysiol.2007.147421. PMID:18202096.
98. Stickland, M.K., Fuhr, D.P., Haykowsky, M.J., Jones, K.E., Paterson, D.I., Ezekowitz, J.A., and McMurtry, M.S. 2011. Carotid chemoreceptor modulation of blood flow during exercise in healthy humans. J. Physiol. 589(24): 6219–6230. doi:10.1113/jphysiol.2011.218099.
99. Svedenhag, J., Wallin, B.G., Sundlof, G., and Henriksson, J. 1984. Skeletal muscle sympathetic activity at rest in trained and untrained subjects. Acta Physiol. Scand. 120: 499–504. doi:10.1111/j.1748-1716.1984.tb07413.x.
100. Task Force of European Society of Cardiology and North American Society of Pacing and Electrophysiology. 1996. Heart rate variability: standards of meaurements, physiological interpretation, and clinical use. Circulation, 93:1043–1065. doi:10.1161/01.CIR.93.5.1043.
101. Usui, K., Bradley, T.D., Spaak, J., Ryan, C.M., Kubo, T., Kaneko, Y., and Floras, J.S. 2005. Inhibition of awake sympathetic nerve activity of heart failure patients with obstructive sleep apnea by nocturnal continuous positive airway pressure. J. Am. Coll. Cardiol. 45: 2008–2011. doi:10.1016/j.jacc.2004.12.080.
102. Valbo, A.B., Hagbarth, K.E., Torebjork, H.E., and Wallin, B.G. 1979. Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. Physiol. Rev. 59: 919–957. PMID:227005.
103. Valbo, A.B., Hagbarth, K.E., and Wallin, B.G. 2004. Microneurography: how the technique developed and its role in the investigation of the sympathetic nervoussystem. J.Appl.Physiol.96:1262–1269.doi:10.1152/japplphysiol.00470.2003.
104. Victor, R.G., Seals, D.R., and Mark, A.L. 1987. Differential control of heart rate and sympathetic nerve activity during dynamic exercise. Insight from intraneural recordings in humans. J. Clin. Invest. 79: 508–516. doi:10.1172/JCI112841.