Advertisement

Clinical Autonomic Research

, Volume 27, Issue 3, pp 157–165 | Cite as

Neural control of blood pressure in women: differences according to age

  • Ana B. PeinadoEmail author
  • Ronee E. Harvey
  • Emma C. Hart
  • Nisha Charkoudian
  • Timothy B. Curry
  • Wayne T. Nicholson
  • B. Gunnar Wallin
  • Michael J. Joyner
  • Jill N. Barnes
Research Article

Abstract

Purpose

The blood pressure “error signal” represents the difference between an individual’s mean diastolic blood pressure and the diastolic blood pressure at which 50% of cardiac cycles are associated with a muscle sympathetic nerve activity burst (the “T50”). In this study we evaluated whether T50 and the error signal related to the extent of change in blood pressure during autonomic blockade in young and older women, to study potential differences in sympathetic neural mechanisms regulating blood pressure before and after menopause.

Methods

We measured muscle sympathetic nerve activity and blood pressure in 12 premenopausal (25 ± 1 years) and 12 postmenopausal women (61 ± 2 years) before and during complete autonomic blockade with trimethaphan camsylate.

Results

At baseline, young women had a negative error signal (−8 ± 1 versus 2 ± 1 mmHg, p < 0.001; respectively) and lower muscle sympathetic nerve activity (15 ± 1 versus 33 ± 3 bursts/min, p < 0.001; respectively) than older women. The change in diastolic blood pressure after autonomic blockade was associated with baseline T50 in older women (r = −0.725, p = 0.008) but not in young women (r = −0.337, p = 0.29). Women with the most negative error signal had the lowest muscle sympathetic nerve activity in both groups (young: r = 0.886, p < 0.001; older: r = 0.870, p < 0.001).

Conclusions

Our results suggest that there are differences in baroreflex control of muscle sympathetic nerve activity between young and older women, using the T50 and error signal analysis. This approach provides further information on autonomic control of blood pressure in women.

Keywords

Aging Baroreflex function Menopause Sympathetic nerve activity 

Notes

Acknowledgements

We thank Shelly Roberts, Sarah Wolhart, Luke Matzek, Alexander Allen, Casey Hines, Pamela Engrav, Nancy Meyer, and Christopher Johnson for their continued assistance throughout the project.

Compliance with ethical standards

Grants

This work was supported by National Institutes of Health grants RR024150 (Center for Translational Science Activities), AG038067 (Jill N. Barnes), HL083947 (B. Gunnar Wallin, Nisha Charkoudian, Michael J. Joyner), American Heart Association grant 2170087 (Emma C. Hart) and Mobility Grant Abroad “José Castillejo” for Young PhD CAS14/00239 (Ana B. Peinado).

Conflict of interest

No conflicts of interest, financial or otherwise, are declared by the authors.

References

  1. 1.
    Burt VL, Whelton P, Roccella EJ, Brown C, Cutler JA, Higgins M, Horan MJ, Labarthe D (1995) Prevalence of hypertension in the US adult population. Results from the Third National Health and Nutrition Examination Survey, 1988–1991. Hypertension 25(3):305–313CrossRefPubMedGoogle Scholar
  2. 2.
    Narkiewicz K, Phillips BG, Kato M, Hering D, Bieniaszewski L, Somers VK (2005) Gender-selective interaction between aging, blood pressure, and sympathetic nerve activity. Hypertension 45(4):522–525CrossRefPubMedGoogle Scholar
  3. 3.
    Mercuro G, Podda A, Pitzalis L, Zoncu S, Mascia M, Melis GB, Rosano GM (2000) Evidence of a role of endogenous estrogen in the modulation of autonomic nervous system. Am J Cardiol 85(6):787–789CrossRefPubMedGoogle Scholar
  4. 4.
    Hart EC, Charkoudian N, Wallin BG, Curry TB, Eisenach J, Joyner MJ (2011) Sex and ageing differences in resting arterial pressure regulation: the role of the beta-adrenergic receptors. J Physiol 589(Pt 21):5285–5297CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Saleh MC, Connell BJ, Saleh TM (2000) Medullary and intrathecal injections of 17 beta-estradiol in male rats. Brain Res 867(1–2):200–209CrossRefPubMedGoogle Scholar
  6. 6.
    Saleh TM, Connell BJ (2000) 17 beta-estradiol modulates baroreflex sensitivity and autonomic tone of female rats. J Auton Nerv Syst 80(3):148–161CrossRefPubMedGoogle Scholar
  7. 7.
    Minson CT, Halliwill JR, Young TM, Joyner MJ (2000) Influence of the menstrual cycle on sympathetic activity, baroreflex sensitivity, and vascular transduction in young women. Circulation 101(8):862–868CrossRefPubMedGoogle Scholar
  8. 8.
    Harvey RE, Barnes JN, Charkoudian N, Curry TB, Eisenach JH, Hart EC, Joyner MJ (2014) Forearm vasodilator responses to a beta-adrenergic receptor agonist in premenopausal and postmenopausal women. Physiol Rep 2(6):1–6CrossRefGoogle Scholar
  9. 9.
    Moreau KL, Donato AJ, Tanaka H, Jones PP, Gates PE, Seals DR (2003) Basal leg blood flow in healthy women is related to age and hormone replacement therapy status. J Physiol 547(Pt 1):309–316CrossRefPubMedGoogle Scholar
  10. 10.
    Barnes JN, Hart EC, Curry TB, Nicholson WT, Eisenach JH, Wallin BG, Charkoudian N, Joyner MJ (2014) Aging enhances autonomic support of blood pressure in women. Hypertension 63(2):303–308CrossRefPubMedGoogle Scholar
  11. 11.
    Hart EC, Joyner MJ, Wallin BG, Karlsson T, Curry TB, Charkoudian N (2010) Baroreflex control of muscle sympathetic nerve activity: a nonpharmacological measure of baroreflex sensitivity. Am J Physiol Heart Circ Physiol 298(3):H816–H822CrossRefPubMedGoogle Scholar
  12. 12.
    Querido JS, Wehrwein EA, Hart EC, Charkoudian N, Henderson WR, Sheel AW (2011) Baroreflex control of muscle sympathetic nerve activity as a mechanism for persistent sympathoexcitation following acute hypoxia in humans. Am J Physiol Regul Integr Comp Physiol 301(6):R1779–R1785CrossRefPubMedGoogle Scholar
  13. 13.
    Wehrwein EA, Joyner MJ, Hart EC, Wallin BG, Karlsson T, Charkoudian N (2010) Blood pressure regulation in humans: calculation of an “error signal” in control of sympathetic nerve activity. Hypertension 55(2):264–269CrossRefPubMedGoogle Scholar
  14. 14.
    Charkoudian N, Joyner MJ, Johnson CP, Eisenach JH, Dietz NM, Wallin BG (2005) Balance between cardiac output and sympathetic nerve activity in resting humans: role in arterial pressure regulation. J Physiol 568(Pt 1):315–321CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Osborn JW, Jacob F, Guzman P (2005) A neural set point for the long-term control of arterial pressure: beyond the arterial baroreceptor reflex. Am J Physiol Regul Integr Comp Physiol 288(4):R846–R855CrossRefPubMedGoogle Scholar
  16. 16.
    Osborn JW (2005) Hypothesis: set-points and long-term control of arterial pressure. A theoretical argument for a long-term arterial pressure control system in the brain rather than the kidney. Clin Exp Pharmacol Physiol 32(5–6):384–393CrossRefPubMedGoogle Scholar
  17. 17.
    Gracia CR, Sammel MD, Freeman EW, Lin H, Langan E, Kapoor S, Nelson DB (2005) Defining menopause status: creation of a new definition to identify the early changes of the menopausal transition. Menopause 12(2):128–135CrossRefPubMedGoogle Scholar
  18. 18.
    Sundlof G, Wallin BG (1977) The variability of muscle nerve sympathetic activity in resting recumbent man. J Physiol 272(2):383–397CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Wilkins BW, Hesse C, Sviggum HP, Nicholson WT, Moyer TP, Joyner MJ, Eisenach JH (2007) Alternative to ganglionic blockade with anticholinergic and alpha-2 receptor agents. Clin Auton Res 17(2):77–84CrossRefPubMedGoogle Scholar
  20. 20.
    Kienbaum P, Karlssonn T, Sverrisdottir YB, Elam M, Wallin BG (2001) Two sites for modulation of human sympathetic activity by arterial baroreceptors? J Physiol 531(Pt 3):861–869CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Wesseling KH, Jansen JR, Settels JJ, Schreuder JJ (1993) Computation of aortic flow from pressure in humans using a nonlinear, three-element model. J Appl Physiol 74(5):2566–2573PubMedGoogle Scholar
  22. 22.
    Wallin BG, Delius W, Sundlof G (1974) Human muscle nerve sympathetic activity in cardiac arrhythmias. Scand J Clin Lab Invest 34(4):293–300CrossRefPubMedGoogle Scholar
  23. 23.
    Saleh TM, Connell BJ (2007) Role of oestrogen in the central regulation of autonomic function. Clin Exp Pharmacol Physiol 34(9):827–832CrossRefPubMedGoogle Scholar
  24. 24.
    Christou DD, Jones PP, Jordan J, Diedrich A, Robertson D, Seals DR (2005) Women have lower tonic autonomic support of arterial blood pressure and less effective baroreflex buffering than men. Circulation 111(4):494–498CrossRefPubMedGoogle Scholar
  25. 25.
    Barnes JN, Matzek LJ, Charkoudian N, Joyner MJ, Curry TB, Hart EC (2012) Association of cardiac baroreflex sensitivity with blood pressure transients: influence of sex and menopausal status. Front Physiol 3:1–6CrossRefGoogle Scholar
  26. 26.
    Convertino VA (1998) Gender differences in autonomic functions associated with blood pressure regulation. Am J Physiol 275(6 Pt 2):R1909–R1920PubMedGoogle Scholar
  27. 27.
    Shoemaker JK, Hogeman CS, Khan M, Kimmerly DS, Sinoway LI (2001) Gender affects sympathetic and hemodynamic response to postural stress. Am J Physiol Heart Circ Physiol 281(5):H2028–H2035PubMedGoogle Scholar
  28. 28.
    Hart EC, Joyner MJ, Wallin BG, Charkoudian N (2012) Sex, ageing and resting blood pressure: gaining insights from the integrated balance of neural and haemodynamic factors. J Physiol 590(Pt 9):2069–2079CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Sundlof G, Wallin BG (1978) Human muscle nerve sympathetic activity at rest. Relationship to blood pressure and age. J Physiol 274:621–637CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Vaccaro A, Despas F, Delmas C, Lairez O, Lambert E, Lambert G, Labrunee M, Guiraud T, Esler M, Galinier M, Senard JM, Pathak A (2014) Direct evidences for sympathetic hyperactivity and baroreflex impairment in Tako Tsubo cardiopathy. PLoS One 9(3):e93278CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Ana B. Peinado
    • 1
    Email author
  • Ronee E. Harvey
    • 2
  • Emma C. Hart
    • 3
  • Nisha Charkoudian
    • 4
  • Timothy B. Curry
    • 2
  • Wayne T. Nicholson
    • 2
  • B. Gunnar Wallin
    • 5
  • Michael J. Joyner
    • 2
  • Jill N. Barnes
    • 2
    • 6
  1. 1.LFE Research Group, Department of Health and Human PerformanceTechnical University of MadridMadridSpain
  2. 2.Department of AnesthesiologyMayo ClinicRochesterUSA
  3. 3.School of Physiology and PharmacologyUniversity of BristolBristolUK
  4. 4.Thermal and Mountain Medicine DivisionUS Army Research Institute of Environmental MedicineNatickUSA
  5. 5.Institute of Neuroscience and PhysiologyThe Sahlgren Academy at Gothenburg UniversityGotheborgSweden
  6. 6.Department of KinesiologyUniversity of Wisconsin-MadisonMadisonUSA

Personalised recommendations