Skip to main content
SpringerLink
Log in

Effects of aging and exercise training on the dynamics of vasoconstriction in skeletal muscle resistance vessels

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

It is unknown whether aging or exercise training affect the dynamics of arteriolar vasoconstriction.

Purpose

We hypothesized that old age will slow, and exercise training will speed, the dynamics of skeletal muscle arteriolar vasoconstriction in resistance vessels of aged rats.

Method

Young (6 month old) and aged (24 month old) male Fischer-344 rats were assigned to sedentary (Sed: n = 6/age group) or exercise-trained (ET: n = 5 aged and 6 young; via treadmill running for 10–12 weeks) groups. After completion of training, arterioles from the red portion of the gastrocnemius muscle were removed, cannulated, and exposed to 10−4 M norepinephrine (NE) or 20 mM caffeine. Changes in luminal diameter were recorded for analysis of constrictor dynamics.

Result

Old age blunted all kinetic parameters (i.e., time delay, time constant) resulting in vasoconstriction taking ~3 times as long to reach a steady state (SS) versus younger counterparts for NE (aged-sed: 15.6 ± 6.0 versus young-sed: 4.6 ± 0.5 s; P < 0.05) with a similar time course to caffeine. Exercise training resulted in a similar time to SS between age groups for NE (aged-ET: 6.8 ± 1.6 versus young-ET: 7.0 ± 0.6 s) and caffeine (aged-ET: 7.8 ± 0.6 versus young-ET: 8.6 ± 1.0 s).

Conclusion

The results of this study demonstrate that aging blunts the rate of vasoconstriction in skeletal muscle resistance vessels to the sympathetic neurotransmitter NE due, in part, to an attenuated rate of contraction from intracellular calcium release. Further, exercise training speeds the dynamics of constriction to both NE and caffeine with old age.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

CSA:

Citrate synthase activity

ET:

Exercise trained

MRT:

Mean response time

NE:

Norepinephrine

Sed:

Sedentary

SS:

Steady state

SV:

Stroke volume

SVR:

Systemic vascular resistance

TD:

Time delay

τ :

Time constant

References

  • Alnaqeeb MA, Goldspink G (1987) Changes in fibre type, number and diameter in developing and ageing skeletal muscle. J Anat 153:31–45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arbeille P, Achaibou F, Fomina G, Pottier JM, Porcher M (1996a) Regional blood flow in microgravity: adaptation and deconditioning. Med Sci Sports Exerc 28(10 Suppl):S70–S79

  • Arbeille P, Fomina G, Pottier J, Porcher M, Coulon J, Kotovskaya A, Poliakov V (1996b) Hemodynamic response to LBNP during the 14 month MIR spaceflight (94–95). J Gravit Physiol 3(2):95–96

  • Behnke BJ, Delp MD (2010) Ageing blunts the dynamics of vasodilation in isolated skeletal muscle resistance vessels. J Appl Physiol (1985) 108 (1):14–20. doi:10.1152/japplphysiol.00970.2009

    Article  CAS  Google Scholar 

  • Behnke BJ, Kindig CA, Musch TI, Koga S, Poole DC (2001) Dynamics of microvascular oxygen pressure across the rest-exercise transition in rat skeletal muscle. Respir Physiol 126(1):53–63

    Article  CAS  Google Scholar 

  • Behnke BJ, Delp MD, Dougherty PJ, Musch TI, Poole DC (2005) Effects of ageing on microvascular oxygen pressures in rat skeletal muscle. Respir Physiol Neurobiol 146(2–3):259–268. doi:10.1016/j.resp.2004.12.009

    Article  PubMed  Google Scholar 

  • Behnke BJ, Armstrong RB, Delp MD (2011) Adrenergic control of vascular resistance varies in muscles composed of different fiber types: influence of the vascular endothelium. Am J Physiol Regul Integr Comp Physiol 301(3):R783–R790. doi:10.1152/ajpregu.00205.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behnke BJ, Ramsey MW, Stabley JN, Dominguez JM, 2nd, Davis RT, 3rd, McCullough DJ, Muller-Delp JM, Delp MD (2012) Effects of ageing and exercise training on skeletal muscle blood flow and resistance artery morphology. J Appl Physiol (1985) 113 (11):1699–1708. doi:10.1152/japplphysiol.01025.2012

    Article  CAS  Google Scholar 

  • Buckey JC, Jr., Lane LD, Levine BD, Watenpaugh DE, Wright SJ, Moore WE, Gaffney FA, Blomqvist CG (1996) Orthostatic intolerance after spaceflight. J Appl Physiol (1985) 81(1):7–18

    Article  Google Scholar 

  • Colleran PN, Behnke BJ, Wilkerson MK, Donato AJ, Delp MD (2008) Simulated microgravity alters rat mesenteric artery vasoconstrictor dynamics through an intracellular Ca(2+) release mechanism. Am J Physiol Regul Integr Comp Physiol 294(5):R1577–R1585. doi:10.1152/ajpregu.00084.2008

    Article  CAS  PubMed  Google Scholar 

  • Copp SW, Ferreira LF, Herspring KF, Musch TI, Poole DC (2009) The effects of ageing on capillary hemodynamics in contracting rat spinotrapezius muscle. Microvasc Res 77(2):113–119. doi:10.1016/j.mvr.2008.11.001

    Article  PubMed  Google Scholar 

  • Davis RT, 3rd, Stabley JN, Dominguez JM, 2nd, Ramsey MW, McCullough DJ, Lesniewski LA, Delp MD, Behnke BJ (2013) Differential effects of ageing and exercise on intra-abdominal adipose arteriolar function and blood flow regulation. J Appl Physiol (1985) 114(6):808–815. doi:10.1152/japplphysiol.01358.2012

    Article  Google Scholar 

  • Davy KP, Seals DR, Tanaka H (1998) Augmented cardiopulmonary and integrative sympathetic baroreflexes but attenuated peripheral vasoconstriction with age. Hypertension 32(2):298–304

    Article  CAS  Google Scholar 

  • del Corsso C, Ostrovskaya O, McAllister CE, Murray K, Hatton WJ, Gurney AM, Spencer NJ, Wilson SM (2006) Effects of ageing on Ca2 + signaling in murine mesenteric arterial smooth muscle cells. Mech Ageing Dev 127(4):315–323. doi:10.1016/j.mad.2005.12.001

    Article  CAS  PubMed  Google Scholar 

  • Delp MD, Duan C (1996) Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J Appl Physiol (1985) 80(1):261–270

    Article  CAS  Google Scholar 

  • Dominguez JM 2nd, Prisby RD, Muller-Delp JM, Allen MR, Delp MD (2010) Increased nitric oxide-mediated vasodilation of bone resistance arteries is associated with increased trabecular bone volume after endurance training in rats. Bone 46(3):813–819. doi:10.1016/j.bone.2009.10.029

    Article  CAS  PubMed  Google Scholar 

  • Donato AJ, Lesniewski LA, Delp MD (2007) Ageing and exercise training alter adrenergic vasomotor responses of rat skeletal muscle arterioles. J Physiol 579(Pt 1):115–125. doi:10.1113/jphysiol.2006.120055

    Article  CAS  Google Scholar 

  • Ghosh P, Mora Solis FR, Dominguez JM, 2nd, Spier SA, Donato AJ, Delp MD, Muller-Delp JM (2015) Exercise training reverses ageing-induced impairment of myogenic constriction in skeletal muscle arterioles. J Appl Physiol (1985) 118(7):904–911. doi:10.1152/japplphysiol.00277.2014

    Article  CAS  Google Scholar 

  • Gollasch M (2012) Vasodilator signals from perivascular adipose tissue. Br J Pharmacol 165(3):633–642. doi:10.1111/j.1476-5381.2011.01430.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanna MA, Taylor CR, Chen B, La HS, Maraj JJ, Kilar CR, Behnke BJ, Delp MD, Muller-Delp JM (2014) Structural remodeling of coronary resistance arteries: effects of age and exercise training. J Appl Physiol (1985) 117(6):616–623. doi:10.1152/japplphysiol.01296.2013

    Article  Google Scholar 

  • Hargens AR, Watenpaugh DE (1996) Cardiovascular adaptation to spaceflight. Med Sci Sports Exerc 28(8):977–982

    Article  CAS  Google Scholar 

  • Hill-Eubanks DC, Werner ME, Heppner TJ, Nelson MT (2011) Calcium signaling in smooth muscle. Cold Spring Harb Perspect Biol 3(9):a004549. doi:10.1101/cshperspect.a004549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hogikyan RV, Supiano MA (1994) Arterial alpha-adrenergic responsiveness is decreased and SNS activity is increased in older humans. Am J Physiol 266(5 Pt 1):E717–E724

    CAS  PubMed  Google Scholar 

  • Ingram DK (2000) Age-related decline in physical activity: generalization to nonhumans. Med Sci Sports Exerc 32(9):1623–1629

    Article  CAS  Google Scholar 

  • Iriuchijima J, Kawaue Y, Teranishi Y (1982) Blood flow redistribution in the transposition response of the rat. Jpn J Physiol 32(5):807–816

    Article  CAS  Google Scholar 

  • Jasperse JL, Woodman CR, Price EM, Hasser EM, Laughlin MH (1999) Hindlimb unweighting decreases ecNOS gene expression and endothelium-dependent dilation in rat soleus feed arteries. J Appl Physiol (1985) 87(4):1476–1482

    Article  CAS  Google Scholar 

  • Kenney WL, Zappe DH (1994) Effect of age on renal blood flow during exercise. Ageing (Milano) 6(4):293–302

    CAS  Google Scholar 

  • Lakatta EG, Wang M, Najjar SS (2009) Arterial ageing and subclinical arterial disease are fundamentally intertwined at macroscopic and molecular levels. Med Clin North Am 93(3):583–604. doi:10.1016/j.mcna.2009.02.008 (Table of contents)

    Article  CAS  Google Scholar 

  • Laughlin MH, Armstrong RB (1983) Rat muscle blood flows as a function of time during prolonged slow treadmill exercise. Am J Physiol 244(6):H814–H824

    CAS  PubMed  Google Scholar 

  • Laughlin MH, Davis MJ, Secher NH, van Lieshout JJ, Arce-Esquivel AA, Simmons GH, Bender SB, Padilla J, Bache RJ, Merkus D, Duncker DJ (2012) Peripheral circulation. Compr Physiol 2(1):321–447. doi:10.1002/cphy.c100048

    Article  PubMed  Google Scholar 

  • Luttrell MJ, Seawright JW, Wilson E, Woodman CR (2013) Effect of age and exercise training on protein:protein interactions among eNOS and its regulatory proteins in rat aortas. Eur J Appl Physiol 113(11):2761–2768. doi:10.1007/s00421-013-2715-7

    Article  CAS  PubMed  Google Scholar 

  • Mahler M (1985) First-order kinetics of muscle oxygen consumption, and an equivalent proportionality between QO2 and phosphorylcreatine level. Implications for the control of respiration. J Gen Physiol 86(1):135–165

    Article  CAS  Google Scholar 

  • Mazzeo RS, Horvath SM (1986) Effects of training on weight, food intake, and body composition in ageing rats. Am J Clin Nutr 44(6):732–738

    Article  CAS  Google Scholar 

  • McCullough DJ, Davis RT, 3rd, Dominguez JM, 2nd, Stabley JN, Bruells CS, Behnke BJ (2011) Effects of ageing and exercise training on spinotrapezius muscle microvascular PO2 dynamics and vasomotor control. J Appl Physiol (1985) 110(3):695–704. doi:10.1152/japplphysiol.01084.2010

    Article  Google Scholar 

  • Miljkovic N, Lim JY, Miljkovic I, Frontera WR (2015) Ageing of skeletal muscle fibers. Annals of rehabilitation medicine 39(2):155–162. doi:10.5535/arm.2015.39.2.155

    Article  PubMed  PubMed Central  Google Scholar 

  • Muller-Delp JM (2016) Heterogeneous ageing of skeletal muscle microvascular function. J Physiol 594(8):2285–2295. doi:10.1113/JP271005

    Article  CAS  PubMed  Google Scholar 

  • Muller-Delp J, Spier SA, Ramsey MW, Lesniewski LA, Papadopoulos A, Humphrey JD, Delp MD (2002a) Effects of ageing on vasoconstrictor and mechanical properties of rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 282(5):H1843–H1854. doi:10.1152/ajpheart.00666.2001

  • Muller-Delp JM, Spier SA, Ramsey MW, Delp MD (2002b) Ageing impairs endothelium-dependent vasodilation in rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 283(4):H1662–H1672. doi:10.1152/ajpheart.00004.2002

  • Mulvagh SL, Charles JB, Riddle JM, Rehbein TL, Bungo MW (1991) Echocardiographic evaluation of the cardiovascular effects of short-duration spaceflight. J Clin Pharmacol 31(10):1024–1026

    Article  CAS  Google Scholar 

  • Musch TI, McAllister RM, Symons JD, Stebbins CL, Hirai T, Hageman KS, Poole DC (2001) Effects of nitric oxide synthase inhibition on vascular conductance during high speed treadmill exercise in rats. Exp Physiol 86(6):749–757

    Article  CAS  Google Scholar 

  • Musch TI, Eklund KE, Hageman KS, Poole DC (2004) Altered regional blood flow responses to submaximal exercise in older rats. J Appl Physiol (1985) 96(1):81–88. doi:10.1152/japplphysiol.00729.2003

    Article  Google Scholar 

  • Ramsey MW, Behnke BJ, Prisby RD, Delp MD (2007) Effects of ageing on adipose resistance artery vasoconstriction: possible implications for orthostatic blood pressure regulation. J Appl Physiol (1985) 103(5):1636–1643. doi:10.1152/japplphysiol.00637.2007

    Article  Google Scholar 

  • Raven PB, Pawelczyk JA (1993) Chronic endurance exercise training: a condition of inadequate blood pressure regulation and reduced tolerance to LBNP. Med Sci Sports Exerc 25(6):713–721

    CAS  PubMed  Google Scholar 

  • Seawright JW, Trache A, Wilson E, Woodman CR (2016) Short-duration increases in intraluminal pressure improve vasoconstrictor responses in aged skeletal muscle feed arteries. Eur J Appl Physiol 116(5):931–937. doi:10.1007/s00421-016-3350-x

    Article  PubMed  Google Scholar 

  • Shipley RD, Muller-Delp JM (2005) Ageing decreases vasoconstrictor responses of coronary resistance arterioles through endothelium-dependent mechanisms. Cardiovasc Res 66(2):374–383. doi:10.1016/j.cardiores.2004.11.005

    Article  CAS  PubMed  Google Scholar 

  • Sindler AL, Delp MD, Reyes R, Wu G, Muller-Delp JM (2009) Effects of ageing and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J Physiol 587(Pt 15):3885–3897. doi:10.1113/jphysiol.2009.172221

    Article  CAS  Google Scholar 

  • Sinkler SY, Segal SS (2014) Ageing alters reactivity of microvascular resistance networks in mouse gluteus maximus muscle. Am J Physiol Heart Circ Physiol 307(6):H830–H839. doi:10.1152/ajpheart.00368.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith EG, Voyles WF, Kirby BS, Markwald RR, Dinenno FA (2007) Ageing and leg postjunctional alpha-adrenergic vasoconstrictor responsiveness in healthy men. J Physiol 582(Pt 1):63–71. doi:10.1113/jphysiol.2007.130591

    Article  CAS  Google Scholar 

  • Society AP (2006) Resource book for the design of animal exercise protocols. https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&ved=0ahUKEwjmtoqym5_QAhUqr1QKHcF1Aj0QFggdMAA&url=http%3A%2F%2Fwww.the-aps.org%2Fmm%2FSciencePolicy%2FAnimalResearch%2FPublications%2FAnimal-Exercise-Protocols%2Fbook14824.pdf&usg=AFQjCNGRC11TiElqof3WQoPtwg8FwEN5KQ. Accessed Jan 2013

  • Spier SA, Delp MD, Meininger CJ, Donato AJ, Ramsey MW, Muller-Delp JM (2004) Effects of ageing and exercise training on endothelium-dependent vasodilatation and structure of rat skeletal muscle arterioles. J Physiol 556(Pt 3):947–958. doi:10.1113/jphysiol.2003.060301

    Article  CAS  Google Scholar 

  • Srere P (1969) Citrate synthase. In: Methods in enzymology, vol XIII. pp 1–11

  • Staron RS, Hagerman FC, Hikida RS, Murray TF, Hostler DP, Crill MT, Ragg KE, Toma K (2000) Fiber type composition of the vastus lateralis muscle of young men and women. J Histochem Cytochem 48(5):623–629

    Article  CAS  Google Scholar 

  • Tumer N, Toklu HZ, Muller-Delp JM, Oktay S, Ghosh P, Strang K, Delp MD, Scarpace PJ (2014) The effects of ageing on the functional and structural properties of the rat basilar artery. Physiol Rep. doi:10.14814/phy2.12031

    Article  PubMed  PubMed Central  Google Scholar 

  • Wieling W, Krediet CT, van Dijk N, Linzer M, Tschakovsky ME (2007) Initial orthostatic hypotension: review of a forgotten condition. Clin Sci (Lond) 112(3):157–165. doi:10.1042/CS20060091

    Article  Google Scholar 

  • Wunsch SA, Muller-Delp J, Delp MD (2000) Time course of vasodilatory responses in skeletal muscle arterioles: role in hyperemia at onset of exercise. Am J Physiol Heart Circ Physiol 279(4):H1715–H1723

    Article  CAS  Google Scholar 

  • Xia N, Li H (2016) The role of perivascular adipose tissue in obesity-induced vascular dysfunction. Br J Pharmacol. doi:10.1111/bph.13650

    Article  PubMed  PubMed Central  Google Scholar 

  • Zebekakis PE, Nawrot T, Thijs L, Balkestein EJ, van der Heijden-Spek J, Van Bortel LM, Struijker-Boudier HA, Safar ME, Staessen JA (2005) Obesity is associated with increased arterial stiffness from adolescence until old age. J Hypertens 23(10):1839–1846

    Article  CAS  Google Scholar 

  • Zou H, Ratz PH, Hill MA (2000) Temporal aspects of Ca(2+) and myosin phosphorylation during myogenic and norepinephrine-induced arteriolar constriction. J Vasc Res 37(6):556–567

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Rahul Verma for assisting with the vessel diameter measures.

Author information

Authors and Affiliations

  1. Department of Kinesiology, Kansas State University, Manhattan, KS, USA

    Elizabeth M. Gittemeier, Steven W. Copp, Alexander B. Opoku-Acheampong & Bradley J. Behnke

  2. Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, FL, USA

    Tyler Ericson

  3. Department of Food, Nutrition and Exercise Sciences, Florida State University, Tallahassee, FL, USA

    Payal Ghosh

  4. Department of Kinesiology, Johnson Cancer Research Center, Kansas State University, Manhattan, KS, 66506, USA

    Bradley J. Behnke

Authors
  1. Elizabeth M. Gittemeier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tyler Ericson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Payal Ghosh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Steven W. Copp
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexander B. Opoku-Acheampong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bradley J. Behnke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bradley J. Behnke.

Ethics declarations

Support

American Cancer Society (BJB) (RSG-14-150-01-CCE).

Conflict of interest

No conflicts of interest, financial or otherwise, are declared by the author(s).

Additional information

Communicated by Fabio Fischetti.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gittemeier, E.M., Ericson, T., Ghosh, P. et al. Effects of aging and exercise training on the dynamics of vasoconstriction in skeletal muscle resistance vessels. Eur J Appl Physiol 117, 397–407 (2017). https://doi.org/10.1007/s00421-017-3541-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-017-3541-0

Keywords

Search

Navigation