Exercise training and sympathetic nervous system activity: Evidence for physical activity dependent neural plasticity

Clinical and Experimental Pharmacology and Physiology

Volumn 34, Issue 4, 2007, Pages 377-384

  Mueller, Patrick J ^a,b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Cardiovascular disease; Exercise; Physical inactivity; Sympathetic nervous system

Indexed keywords

ADRENERGIC SYSTEM; BLOOD PRESSURE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR SYSTEM; CENTRAL NERVOUS SYSTEM; EXERCISE; EXERCISE PHYSIOLOGY; HEART FAILURE; HUMAN; HYPERTENSION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PHYSICAL ACTIVITY; PRESSORECEPTOR REFLEX; REGULATORY MECHANISM; REVIEW;

ANIMALS; HOMEOSTASIS; HUMANS; MODELS, BIOLOGICAL; MOTOR ACTIVITY; NEURONAL PLASTICITY; SYMPATHETIC NERVOUS SYSTEM;

EID: 33846985620     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2007.04590.x     Document Type: Review

References (91)

1. Thom T, Haase N, Rosamond W et al. American heart association statistics committee and stroke statistics subcommittee. Heart disease and stroke statistics, 2006 update: A report from the American heart association statistics committee and stroke statistics subcommittee. Circulation 2006; 113: E85-151.
2. Mokdad AH, Marks JS, Stroup DF, Gerberding JL. Actual causes of death in the United States, 2000. JAMA 2004; 291: 1238-45.
3. Lees SJ, Booth FW. Sedentary death syndrome. Can. J. Appl. Physiol. 2004; 29: 447-60.
4. Julius S, Nesbitt S. Sympathetic overactivity in hypertension. A moving target. Am. J. Hypertens. 1996; 9: 113S-20S.
5. Schlaich MP, Lambert E, Kaye D et al. Sympathetic augmentation in hypertension. Role of nerve firing, norepinephrine reuptake, and angiotensin neuromodulation. Hypertension 2004; 43: 169-75.
6. Cornelissen VA, Fagard RH. Effects of endurance training on blood pressure, blood pressure-regulating mechanisms, and cardiovascular risk factors. Hypertension 2005; 45: 667-75.
7. Billman GE. Aerobic exercise conditioning: A nonpharmacological antiarrhythmic intervention. J. Appl. Physiol. 2002; 92: 446-54.
8. Zucker IH, Patel KP, Schultz HD, Li Y-F, Wang W, Pliquett RU. Exercise training and sympathetic regulation in experimental heart failure. Exerc. Sport Sci. Rev. 2004; 32: 107-11.
9. Tipton CM. Exercise, training, and hypertension: An update. Exerc. Sport Sci. Rev. 1991; 19: 447-505.
10. Meredith IT, Friberg P, Jennings GL et al. Exercise training lowers resting renal but not cardiac sympathetic activity in humans. Hypertension 1991; 18: 575-82.
11. Iwasaki K-I, Zhang R, Zuckerman JH, Levine BD. Dose-response relationship of the cardiovascular adaptation to endurance training in healthy adults: How much training for what benefit? J. Appl. Physiol. 2003; 95: 1575-83.
12. Pescatello LS, Franklin BA, Fagard R, Farquhar WB, Kelley GA, Ray CA. American college of sports medicine position stand. Exercise and hypertension. Med. Sci. Sports Exerc. 2004; 36: 533-53.
13. Roveda F, Middlekauff HR, Rondon MU et al. The effects of exercise training on sympathetic neural activation in advanced heart failure: A randomized controlled trial. J. Am. Coll. Cardiol. 2003; 42: 854-60.
14. De Angelis K, Wichi RB, Jesus WRA et al. Exercise training changes autonomic cardiovascular balance in mice. J. Appl. Physiol. 2004; 96: 2174-8.
15. Negrao C-E, Irigoyen MC, Moreira ED, Brum P-C, Freire PM, Krieger E-M. Effect of exercise training on RSNA, baroreflex control, and blood pressure responsiveness. Am. J. Physiol. 1993; 265: R365-70.
16. Krieger EM, Da Silva GJJ, Negrao CE. Effects of exercise training on baroreflex control of the cardiovascular system. Ann. N.Y. Acad. Sci. 2001; 940: 338-47.
17. Kramer JM, Beatty JA, Plowey ED, Waldrop TG. Exercise and hypertension: A model for central neural plasticity. Clin. Exp. Pharmacol. Physiol. 2002; 29: 122-6.
18. Collins HL, Rodenbaugh DW, DiCarlo SE. Daily exercise attenuates the development of arterial blood pressure related cardiovascular risk factors in hypertensive rats. Clin. Exp. Hypertens. 2000; 22: 193-202.
19. Benedict CR, Shelton B, Johnstone DE et al. Prognostic significance of plasma norepinephrine in patients with asymptomatic left ventricular dysfunction. SOLVD Investigators. Circulation 1996; 94: 690-7.
20. Zoccali C, Mallamaci F, Parlongo S et al. Plasma norepinephrine predicts survival and incident cardiovascular event in patients with end-stage renal disease. Circulation 2002; 105: 1354-9.
21. Ray CA, Hume KM. Sympathetic neural adaptation to exercise training in humans: Insights from microneurography. Med. Sci. Sports Exerc. 1998; 30: 387-91.
22. Jennings G, Nelson L, Nestel P et al. The effects of changes in physical activity on major cardiovascular risk factors, hemodynamics, sympathetic function, and glucose utilization in man: A controlled study of four levels of activity. Circulation 1986; 73: 30-40.
23. Grassi G, Seravalle G, Calhoun DA, Mancia G. Physical training and baroreceptor control of sympathetic nerve activity in humans. Hypertension 1994; 23: 294-301.
24. Ng AV, Callister R, Johnson DG, Seals DR. Endurance exercise training is associated with elevated basal sympathetic nerve activity in healthy older humans. J. Appl. Physiol. 1994; 77: 1366-74.
25. Fadel PJ, Stromstad M, Hansen J et al. Arterial baroreflex control of sympathetic nerve activity during acute hypotension: Effect of fitness. Am. J. Physiol. Heart Circ. Physiol. 2001; 280: H2524-32.
26. Alvarez GE, Halliwill JR, Ballard TP, Beske SD, Davy KP. Sympathetic neural regulation in endurance-trained humans: Fitness vs. fatness. J. Appl. Physiol. 2005; 98: 498-502.
27. Krieger EM, Brum PC, Negrao CE. Influence of exercise training on neurogenic control of blood pressure in spontaneously hypertensive rats. Hypertension 1999; 34: 720-3.
28. DiCarlo SE, Bishop VS. Exercise training enhances cardiac afferent inhibition of baroreflex function. Am. J. Physiol. 1990; 258: H212-20.
29. DiCarlo SE, Bishop VS. Exercise training attenuates baroreflex regulation of nerve activity in rabbits. Am. J. Physiol. 1988; 255: H974-9.
30. Chen CY, DiCarlo SE. Daily exercise and gender influence arterial baroreflex regulation of heart rate and nerve activity. Am. J. Physiol. 1996; 271: H1840-8.
31. Negrao CE, Moreira ED, Brum PC, Denadai MLDR, Krieger EM. Vagal and sympathetic control of heart rate during exercise by sedentary and exercise-trained rats. Braz. J. Med. Biol. Res. 1992; 25: 1045-52.
32. Blair ML, Goodyear NN, Gibbons LW, Cooper KH. Physical fitness and incidence of hypertension in healthy normotensive men and women. JAMA 1984; 252: 487-90.
33. Blair SN, Franklin BA, Jakicic JM, Kibler WB. New vision for health promotion within sports medicine. Am. J. Health Promot. 2003; 18: 182-5.
34. Booth FW, Chakravarthy MV, Gordon SE, Spangenburg EE. Waging war on physical inactivity: Using modern molecular ammunition against an ancient enemy. J. Appl. Physiol. 2002; 93: 3-30.
35. Ang ET, Dawe GS, Wong PT, Moochhala S, Ng YK. Alterations in spatial learning and memory after forced exercise. Brain Res. 2006; 1113: 186-93.
36. Fordyce DE, Farrar RP. Physical effects on hippocampal and parietal cortical cholinergic function and spatial learning in F344 rats. Behav. Brain Res. 1991; 43: 115-23.
37. Fordyce DE, Farrar RP. Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning. Behav. Brain Res. 1991; 46: 123-33.
38. Samorajski T, Delaney C, Durham L, Ordy JM, Johnson JA, Dunlap WP. Effect of exercise on longevity, body weight, locomotor performance, and passive-avoidance memory of C57BL/6J mice. Neurobiol. Aging 1985; 6: 17-24.
39. Anderson BJ, Rapp DN, Baek DH, McCloskey DP, Coburn-Litvak PS, Robinson JK. Exercise influences spatial learning in the radial arm maze. Physiol. Behav. 2000; 70: 425-9.
40. Van Praag H, Christie BR, Sejnowski TJ, Gage FH. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl Acad. Sci. USA 1999; 96: 13 427-31.
41. Farmer J, Zhao X, Van Praag H, Wodtke K, Gage FH, Christie BR. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience 2004; 124: 71-9.
42. Cotman CW, Engesser-Cesar C. Exercise enhances and protects brain function. Exerc. Sport Sci. Rev. 2002; 30: 75-9.
43. Dishman RK, Berthoud H-R, Booth FW et al. Neuobiology of exercise. Obesity 2006; 14: 345-56.
44. Carro E, Nunez A, Busiguina S, Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J. Neurosci. 2000; 20: 2926-33.
45. Jackson K, Vieira Silva HM, Zhang W, Michelini LC, Stern JE. Exercise training differentially affects intrinsic excitability of autonomic and neuroendocrine neurons in the hypothalamic paraventricular nucleus. J. Neurophysiol. 2005: 3211-20.
46. Nelson AJ, Juraska JM, Musch TI, Iwamoto GA. Neuroplastic adaptations to exercise: Neuronal remodeling in cardiorespiratory and locomotor areas. J. Appl. Physiol. 2005; 99: 2312-22.
47. Chen CY, DiCarlo SE, Scislo TJ. Daily spontaneous running attenuated the central gain of the arterial baroreflex. Am. J. Physiol. Heart Circ. Physiol. 1995; 268: H662-9.
48. Scislo TJ, DiCarlo SE, Collins HL. Daily spontaneous running did not alter vagal afferent reactivity. Am. J. Physiol. Heart Circ. Physiol. 1993; 265: H1564-70.
49. Mueller PJ, Hasser EM. 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. 2006; 290: R383-92.
50. DiCarlo SE, Zheng H, Collins HL, Rodenbaugh DW, Patel KP. Daily exercise normalizes the number of diaphorase (NOS) positive neurons in the hypothalamus of hypertensive rats. Brain Res. 2002; 955: 153-60.
51. Zheng H, Li YF, Cornish KG, Zucker IH, Patel KP. Exercise training improves endogenous nitric oxide mechanisms within the paraventricular nucleus in rats with heart failure. Am. J. Physiol. Heart Circ. Physiol. 2005; 288: H2332-41.
52. Mueller PJ, Cunningham JT, Patel KP, Hasser EM. Proposed role of the paraventricular nucleus in cardiovascular deconditioning. Acta Physiol. Scand. 2003; 177: 27-35.
53. Beatty JA, Kramer JM, Plowey ED, Waldrop TG. Physical exercise decreases neuronal activity in the posterior hypothalamic area of spontaneously hypertensive rats. J. Appl. Physiol. 2005; 98: 572-8.
54. Kramer JM, Beatty JA, Little HR, Plowey ED, Waldrop TG. Chronic exercise alters caudal hypothalamic regulation of the cardiovascular system in hypertensive rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001; 280: R389-97.
55. De Souza CG, Michelini LC, Fior-Chadi DR. Receptor changes in the nucleus tractus solitarii of the rat after exercise training. Med. Sci. Sports Exerc. 2001; 33: 1471-6.
56. Martins-Pinge MC, Becker LK, Garcia MR et al. Attenuated pressor responses to amino acids in the rostral ventrolateral medulla after swimming training in conscious rats. Auton. Neurosci. 2005; 122: 21-8.
57. Greenwood BN, Kennedy S, Smith TP, Campeau S, Day HEW, Fleshner M. Voluntary free wheel running selectively modulates catecholamine content in peripheral tissue and c-fos expression in the central sympathetic circuit following exposure to uncontrollable stress in rats. Neuroscience 2003; 120: 269-81.
58. Becker LK, Santos RAS, Campagnole-Santos MJ. Cardiovascular effects of angiotensin II and angiotensin-(1-7) at the RVLM of trained normotensive rats. Brain Res. 2005; 1040: 121-8.
59. Mueller PJ. Exercise training attenuates increases in lumbar sympathetic nerve activity produced by stimulation of the rostral ventrolateral medulla. J. Appl. Physiol. 2007 (in press).
60. Bedford TG, Tipton CM. Exercise training and the arterial baroreflex. J. Appl. Physiol. 1987; 63: 1926-32.
61. Tipton CM, Matthes RD, Bedford TG. Influence of training on the blood pressure changes during lower negative pressure in rats. Med. Sci. Sports Exerc. 1982; 14: 81-90.
62. Paynter DE, Tipton CM, Tcheng TK. Responses of immunosympathectomized rats to training. J. Appl. Physiol. 1977; 42: 935-40.
63. Raven PB, Pawelczyk JA. Chronic endurance exercise training: A condition of inadequate blood pressure regulation and reduced tolerance to LBNP. Med. Sci. Sports Exerc. 1993; 25: 713-21.
64. Ciriello J, Hochstenbach SL, Roder S. Central projections of baroreceptor and chemoreceptor afferent fibers in the rat. In: Barraco IRA (ed.). The Nucleus of the Solitary Tract. CRC Press, Boca Raton. 1994; 35-50.
65. Andresen MC, Kunze DL. Nucleus tractus solitarius: Gateway to neural circulatory control. Annu. Rev. Physiol. 1994; 56: 93-116.
66. Sved AF, Gordon FJ. Amino acids as central neurotransmitters in the baroreceptor reflex pathway. News Physiol. Sci. 1994; 9: 243-5.
67. Sapru HN. Neurotransmitters in the nucleus tractus solitarius mediating cardiovascular function. In: Dun NJ, Machado BH, Pilowsky PM (eds). Neural Mechanisms of Cardiovascular Regulation. Kluwer Academic Publishers, Norwell, MA. 2004; 81-98.
68. Doba N, Reis DJ. Acute fulminating neurogenic hypertension produced by brainstem lesions in the rat. Circ. Res. 1973; 32: 584-93.
69. Talman WT, Perrone MH, Reis DJ. Acute hypertension after the local injection of kainic acid into the nucleus tractus solitarii of rats. Circ. Res. 1981; 48: 292-8.
70. Sved AF, Imaizumi T, Talman WT, Reis DJ. Vasopressin contributes to hypertension caused by nucleus tractus solitarius lesions. Hypertension 1985; 7: 262-7.
71. Schreihofer AM, Sved AF. Nucleus tractus solitarius and control of blood pressure in chronic sinoaortic denervated rats. Am. J. Physiol. 1992; 263: R258-66.
72. Guyenet PG, Stornetta RL. The presympathetic cells of the rostral ventrolateral medulla (RVLM). Anatomy, physiology and role in the control of circulation. In: Dun NJ, Machado BH, Pilowsky PM (eds). Neural Mechanisms of Cardiovascular Regulation. Kluwer Academic Publishers, Norwell, MA. 2004; 187-218.
73. Sved AF, Ito S, Sved JC. Brainstem mechanisms of hypertension: Role of the rostral ventrolateral medulla. Curr. Hypertens. Rep. 2003; 5: 262-8.
74. Dampney RAL. Functional organization of central pathways regulating the cardiovascular system. Physiol. Rev. 1994; 74: 323-64.
75. Morgan JI, Cohen DR, Hempstead JL, Curran T. Mapping patterns of c-fos expression in the central nervous system after seizure. Science 1987; 237: 192-7.
76. Dragunow M, Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 1989; 29: 261-5.
77. Dampney RAL, Polson JW, Potts PD, Hirooka Y, Horiuchi J. Functional organization of brain pathways subserving the baroreceptor reflex: Studies in conscious animals using immediate early gene expression. Cell. Mol. Neurobiol. 2003; 23: 597-616.
78. Mueller PJ, Watson MA, Cunningham JT, Hasser EM. Hypotension-induced fos expression in rostral ventrolateral medulla of exercise trained rats. Med. Sci. Sports Exerc. 2005; 37: S153-4 (Abstract).
79. Potts PD, Polson JW, Hirooka Y, Dampney RAL. Effects of sinoaortic denervation on fos expression in the brain evoked by hypertension and hypotension in conscious rabbits. Neuroscience 1997; 77: 503-20.
80. Li Y-W, Dampney RAL. Expression of Fos-like protein in brain following sustained hypertension and hypotension in conscious rabbits. Neuroscience 1994; 61: 613-34.
81. Curtis KS, Cunningham JT, Heesch CM. Fos expression in brain stem nuclei of pregnant rats after hydralazine-induced hypotension. Am. J. Physiol. 1999; 277: R532-40.
82. Lohmeier TE, Hilderbrandt DA, Warren S, May PJ, Cunningham JT. Recent insights into the interactions between the baroreflex and the kidneys in hypertension. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005; 288: R828-36.
83. Sothmann MS, Buckworth J, Claytor RP, Cox RH, White-Welkley JE, Dishman RK. Exercise training and the cross-stressor adaptation hypothesis. Exerc. Sport Sci. Rev. 1996; 24: 267-87.
84. O'Sullivan SE, Bell C. Training reduces autonomic cardiovascular responses to both exercise-dependent and -independent stimuli in humans. Auton. Neurosci. 2001; 91: 76-84.
85. Morimoto K, Tan N, Nishiyasu T, Sone R, Murakami N. Spontaneous wheel running attenuates cardiovascular responses to stress in rats. Pflügers Arch. 2000; 440: 216-22.
86. Overton JM, Kregel KC, Davis-Gorman G, Seals DR, Tipton CM, Fisher LA. Effects of exercise training on responses to central injection of CRF and noise stress. Physiol. Behav. 1991; 49: 93-8.
87. Bauer RM, Waldrop TG, Iwamoto GA, Holzwarth MA. Properties of ventrolateral medullary neurons that respond to muscular contraction. Brain Res. Bull. 1992; 28: 167-78.
88. Morrison SF, Reis DJ. Reticulospinal vasomotor neurons in the RVL mediate the somatosympathetic reflex. Am. J. Physiol. 1989; 256: R1084-97.
89. Stornetta RL, Morrison SF, Ruggiero DA, Reis DJ. Neurons of rostral ventrolateral medulla mediate somatic pressor reflex. Am. J. Physiol. 1989; 256: R448-62.
90. Kiely JM, Gordon FJ. Non-NMDA receptors in the rostral ventrolateral medulla mediate somatosympathetic pressor responses. J. Auton. Nerv. Syst. 1993; 43: 231-40.
91. Mueller PJ. Blunted centrally mediated sympathoexcitation in exercise trained rats. FASEB J. 2006; 20: A1414 (Abstract).