Physically Active Lifestyle Enhances Vagal-Cardiac Function but Not Central Autonomic Neural Interaction in Elderly Humans

Abstract

The cause of the age-related impairment of arterial baroreflex function remains ill-defined; moreover, it is unknown whether this impairment results from aging per se or from an inactive lifestyle associated with aging. In this study, we sought to: 1) determine whether elderly individuals who maintained an active lifestyle had an enhanced carotid baroreflex function as compared with their sedentary counterparts; and 2) determine whether this difference was due in part to altered function of the arterial baroreceptor and/or altered central modulation. Eight healthy, sedentary (SED, 68 ± 2 yr) and eight physically active (ACT, 68 ± 1 yr) elderly men with peak O₂ consumption 25.5 ± 1.2 vs 35.7 ± 2.4 ml/min/kg (P < 0.01), respectively, were assessed with carotid baroreceptor (CBR) function using 5s pulses of neck pressure or suction (ranging from +40 to −80 Torr) delivered to the carotid sinus region at rest and during lower body negative pressure (LBNP) of −15 and −40 Torr. Changes in heart rate (HR) and mean arterial pressure (MAP) were assessed for CBR-HR and CBR-MAP gains, respectively. Overall CBR-HR gains in a range of ∼ 120 mmHg of carotid sinus pressure were greater (P < 0.01) in ACT than SED at rest and during LBNP. The derived peak CBR-HR slopes between ACT and SED at rest were −0.32 ± 0.07 vs −0.11 ± 0.02 bpm/mmHg (P = 0.007), respectively. However, there was no statistical difference (P = 0.37) in CBR-MAP gains between the groups. Neither CBR-MAP (P = 0.08) nor CBR-HR (P = 0.41) gain was augmented by LBNP in the elderly. Conclusion: Active lifestyle enhances the CBR-HR reflex sensitivity as a result of the improved vagal-cardiac function in elderly people. Aging is associated with an absence of central autonomic interaction in the control of blood pressure regardless of physical fitness.

Get full access to this article

View all access options for this article.

References

Bishop V, Malliani A, Thoren P. Cardiac mechanoreceptors. In: Shepherd JT, Abboud FM, Eds. Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow. Bethesda: American Physiological Society, pp497–555, 1983.

Danson EJ, Paterson DJ. Reactive oxygen species and autonomic regulation of cardiac excitability. J Cardiovasc Electrophysiol 17:S104–S112, 2006.

Duckett S. The normal aging human brain. In: Duckett S, De La Torre JC, Eds. Pathology of the Aging Human Nervous System (2nd ed.). New York: Oxford University Press, pp1–15, 2001.

Ebert T, Smith J, Barney J, Merrill D, Smith G. The use of thoracic impedance for determining thoracic blood volume changes in man. Aviat Space Environ Med 57:49–53, 1986.

Ebert TJ, Eckberg DL, Vetrovec GM, Cowley MJ. Impedance cardiograms reliably estimate beat-by-beat changes of left ventricular stroke volume in humans. Cardiovasc Res 18:354–360, 1984.

Eckberg DL, Cavanaugh MS, Mark AL, Abboud FM. A simplified neck suction device for activation of carotid baroreceptors. J Lab Clin Med 85:167–173, 1975.

Eckberg DL, Sleight P. Human Baroreflexes in Health and Disease. Oxford: Clarendon Press, 1992.

Eskurza I, Monahan KD, Robinson JA, Seals DR. Effect of acute and chronic ascorbic acid on flow-mediated dilatation with sedentary and physically active human ageing. J Physiol 556:315–324, 2004.

Galetta F, Franzoni F, Femia FR, Bartolomucci F, Carpi A, Santoro G. Left ventricular diastolic function and carotid artery wall in elderly athletes and sedentary controls. Biomed Pharmacother 58:437–442, 2004.

10.

Hainsworth R. Reflexes from the heart. Physiol Rev 71:617–658, 1991.

11.

Hunt BE, Farquhar WB, and Taylor JA. Does reduced vascular stiffening fully explain preserved cardiovagal baroreflex function in older, physically active men? Circulation 103:2424–2427, 2001.

12.

Ichinose M, Saito M, Kitano A, Hayashi K, Kondo N, Nishiyasu T. Modulation of arterial baroreflex dynamic response during mild orthostatic stress in humans. J Physiol 557:321–330, 2004.

13.

Johnson SM, Felder RB. Effects of aging on the intrinsic membrane properties of medial NTS neurons of Fischer-344 rats. J Neurophysiol 70:1975–1987, 1993.

14.

Kaushal P, Taylor JA. Inter-relations among declines in arterial distensibility, baroreflex function and respiratory sinus arrhythmia. J Am Coll Cardiol 39:1524–1530, 2002.

15.

Keller DM, Wasmund WL, Wray DW, Ogoh S, Fadel PJ, Smith ML, Raven PB. Carotid baroreflex control of leg vascular conductance at rest and during exercise. J Appl Physiol 94:542–548, 2003.

16.

Korkushko OV, Frolkis MV, Shatilo VB. Reaction of pituitary-adrenal and autonomic nervous systems to stress in trained and untrained elderly people. J Auton Nerv Syst 54:27–32, 1995.

17.

Korner PI. Integrative neural cardiovascular control. Physiol Rev 51: 312–367, 1971.

18.

Kubicek WG, Karnegis JN, Patterson RP, Witsoe DA, Mattson RH. Development and evaluation of an impedance cardiac output system. Aerosp Med 37:1208–1212, 1966.

19.

Loewy AD. Central autonomic pathways. In: Loewy AD, Spyer KM, Eds. Central Regulation of Autonomic Functions. New York: Oxford University Press, pp88–103, 1990.

20.

Loewy AD, Spyer KM. Vagal preganglionic neurons. In: Loewy AD, Spyer KM, Eds. Central Regulation of Autonomic Functions. New York: Oxford University Press, pp68–87, 1990.

21.

Ma X, Abboud FM, Chapleau MW. Analysis of afferent, central, and efferent components of the baroreceptor reflex in mice. Am J Physiol Regul Integr Comp Physiol 283:R1033–1040, 2002.

22.

Mancia G, Lorenz RR, Shepherd JT. Reflex control of circulation by heart and lungs. Int Rev Physiol 9:111–144, 1976.

23.

Mark AL, Mancia G. Cardiopulmonary baroreflexes in humans. In: Shepherd JT, Abboud FM, Eds. Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow. Bethesda: American Physiological Society, pp795–813, 1983.

24.

Monahan KD, Dinenno FA, Seals DR, Clevenger CM, Desouza CA, Tanaka H. Age-associated changes in cardiovagal baroreflex sensitivity are related to central arterial compliance. Am J Physiol Heart Circ Physiol 281:H284–289, 2001.

25.

Monahan KD, Dinenno FA, Tanaka H, Clevenger CM, DeSouza CA, Seals DR. Regular aerobic exercise modulates age-associated declines in cardiovagal baroreflex sensitivity in healthy men. J Physiol 529: 263–271, 2000.

26.

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 290:R383–392, 2006.

27.

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 77:1366–1374, 1994.

28.

Nishiyasu T, Shi X, Mack GW, Nadel ER. Forearm vascular responses to baroreceptor unloading at the onset of dynamic exercise. J Appl Physiol 75:979–985, 1993.

29.

Ogoh S, Fadel PJ, Monteiro F, Wasmund WL, Raven PB. Haemodynamic changes during neck pressure and suction in seated and supine positions. J Physiol 540:707–716, 2002.

30.

Ogoh S, Fisher JP, Dawson EA, White MJ, Secher NH, Raven PB. Autonomic nervous system influence on arterial baroreflex control of heart rate during exercise in humans. J Physiol 566:599–611, 2005.

31.

Okazaki K, Iwasaki KI, Prasad A, Palmer MD, Martini ER, Fu Q, Arbab-Zadeh A, Zhang R, Levine BD. Dose-response relationship of endurance training for autonomic circulatory control in healthy seniors. J Appl Physiol, 2005.

32.

Pawelczyk J, Matzen S, Friedman D, Secher N. Cardiovascular and hormonal responses to central hypovolaemia in humans. In: Secher N, Pawelczyk J, Ludbrook J, Eds. Blood Loss and Shock. London: Edward Arnold, pp25–36, 1994.

33.

Pawelczyk JA, Raven PB. Reductions in central venous pressure improve carotid baroreflex responses in conscious men. Am J Physiol 257:H1389–1395, 1989.

34.

Persson P. Interaction of arterial and cardiopulmonary reflexes. In: Persson P, Kirchheim H. Baroreceptor Reflexes —Integrative functions and clinical aspects. Berlin: Springer-Verlag, pp126–153, 1991.

35.

Potts JT, Shi X, Raven PB. Cardiopulmonary baroreceptors modulate carotid baroreflex control of heart rate during dynamic exercise in humans. Am J Physiol 268:H1567–1576, 1995.

36.

Potts JT, Shi XR, Raven PB. Carotid baroreflex responsiveness during dynamic exercise in humans. Am J Physiol 265:H1928–1938, 1993.

37.

Schmidt RE. The aging autonomic nervous system. In: Duckett S, De La Torre JC, Eds. Pathology of the Aging Human Nervous System (2nd ed.). New York: Oxford University Press, pp527–545, 2001.

38.

Scislo TJ, DiCarlo SE, Collins HL. Daily spontaneous running did not alter vagal afferent reactivity. Am J Physiol 265:H1564–1570, 1993.

39.

Seller H. Central baroreceptor reflex pathways. In: Persson P, Kirchheim H. Baroreceptor Reflexes —Integrative functions and clinical aspects. Berlin: Springer-Verlag, pp45–74, 1991.

40.

Shi X, Gallagher KM, Welch-O’Connor RM, Foresman BH. Arterial and cardiopulmonary baroreflexes in 60- to 69- vs. 18- to 36- yr-old humans. J Appl Physiol 80:1903–1910, 1996.

41.

Shi X, Stevens GH, Foresman BH, Stern SA, Raven PB. Autonomic nervous system control of the heart: endurance exercise training. Med Sci Sports Exerc 27:1406–1413, 1995.

42.

Smith DT, Hoetzer GL, Greiner JJ, Stauffer BL, DeSouza CA. Effects of ageing and regular aerobic exercise on endothelial fibrinolytic capacity in humans. J Physiol 546:289–298, 2003.

43.

Smith ML, Hudson DL, Graitzer HM, Raven PB. Exercise training bradycardia: the role of autonomic balance. Med Sci Sports Exerc 21: 40–44, 1989.

44.

Smith RG, Betancourt L, Sun Y. Molecular endocrinology and physiology of the aging central nervous system. Endocr Rev 26: 203–250, 2005.

45.

Spyer KM. The central nervous organization of reflex circulatory control. In: Loewy AD, Spyer KM, Eds. Central Regulation of Autonomic Functions. New York: Oxford University Press, pp168–188, 1990.

46.

Tanaka H, Davy KP, Seals DR. Cardiopulmonary baroreflex inhibition of sympathetic nerve activity is preserved with age in healthy humans. J Physiol 515:249–254, 1999.

47.

Tanaka H, Seals DR, Monahan KD, Clevenger CM, DeSouza CA, Dinenno FA. Regular aerobic exercise and the age-related increase in carotid artery intima-media thickness in healthy men. J Appl Physiol 92:1458–1464, 2002.

48.

Taylor JA, Halliwill JR, Brown TE, Hayano J, Eckberg DL. ‘Non-hypotensive’ hypovolaemia reduces ascending aortic dimensions in humans. J Physiol 483:289–298, 1995.

49.

Thomas SH. Impedance cardiography using the Sramek-Bernstein method: accuracy and variability at rest and during exercise. Br J Clin Pharmacol 34:467–476, 1992.

50.

Tsutsui Y, Sagawa S, Yamauchi K, Endo Y, Yamazaki F, Shiraki K. Cardiovascular responses to lower body negative pressure in the elderly: role of reduced leg compliance. Gerontology 48:133–139, 2002.

51.

Victor RG and Mark AL. Interaction of cardiopulmonary and carotid baroreflex control of vascular resistance in humans. J Clin Invest 76: 1592–1598, 1985.

52.

Wray DW, Formes KJ, Weiss MS, O-Yurvati AH, Raven PB, Zhang R, Shi X. Vagal cardiac function and arterial blood pressure stability. Am J Physiol 281:H1870–H1880, 2001.