Abstract
Purpose
This study tested the hypothesis that blood pressure responses would increase relative to force production in response to prolonged bouts of muscular work.
Methods
Fifteen individuals performed two minutes of static handgrip (SHG; 35% MVC), followed by three minutes of post-exercise-cuff-occlusion (PECO), before and after thirty minutes of rest (control), or rhythmic handgrip exercise (RHG) of the contralateral and ipsilateral forearms. Beat-by-beat recordings of mean arterial pressure (MAP), heart rate (HR), and handgrip force (kg) were averaged across one-minute periods at baseline, and minutes 5, 10, 15, 20, 25, and 30 of RHG. MAP was also normalized to handgrip force, providing a relative measure of exercise pressor responses (mmHg/kg). Hemodynamic responses to SHG and PECO were also compared before and after contralateral RHG, ipsilateral RHG, and control, respectively. Similar to the RHG trial, areas under the curve were calculated for MAP (blood pressure index; BPI) and normalized to the time tension index (BPInorm).
Results
HR and MAP significantly increased during RHG (15.3 ± 1.4% and 20.4 ± 3.2%, respectively, both p < 0.01), while force output decreased by up to 36.6 ± 8.0% (p < 0.01). This resulted in a 51.6 ± 9.4% increase in BPInorm during 30 min of RHG (p < 0.01). In contrast, blood pressure responses to SHG and PECO were unchanged following RHG (all p ≥ 0.07), and only the mean HR (4.2 ± 1.5%, p = 0.01) and ΔHR (67.2 ± 18.1%, p < 0.01) response to SHG were exaggerated following ipsilateral RHG.
Conclusions
The magnitude of exercise pressor responses relative to force production progressively increases during, but not following, prolonged bouts of muscular work.
Similar content being viewed by others
Data availability
The datasets generated and/or analyzed during the current study are not publicly available due to data sharing policies of the host institution. However, data may be made available by the corresponding author upon reasonable request, and with the permission of the University of Southern Mississippi.
References
Allen DG, Kabbara AA, Westerblad H (2002) Muscle fatigue: the role of intracellular calcium stores. Can J Appl Physiol 27(1):83–96. https://doi.org/10.1139/h02-006
Alway SE, Hughson RL, Green HJ, Patla AE, Frank JS (1987) Twitch potentiation after fatiguing exercise in man. Eur J Appl Physiol Occup Physiol 56(4):461–466. https://doi.org/10.1007/bf00417776
Amann M, Dempsey JA (2008) Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol 586(1):161–173. https://doi.org/10.1113/jphysiol.2007.141838
Amann M, Proctor LT, Sebranek JJ, Eldridge MW, Pegelow DF, Dempsey JA (2008) Somatosensory feedback from the limbs exerts inhibitory influences on central neural drive during whole body endurance exercise. J Appl Physiol 105(6):1714–1724. https://doi.org/10.1152/japplphysiol.90456.2008
Amann M, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA (2009) Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 587(1):271–283. https://doi.org/10.1113/jphysiol.2008.163303
Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA (2010) Group III and IV muscle afferents contribute to ventilatory and cardiovascular response to rhythmic exercise in humans. J Appl Physiol 109(4):966–976. https://doi.org/10.1152/japplphysiol.00462.2010
Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA (2011) Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. J Physiol 589(Pt 21):5299–5309. https://doi.org/10.1113/jphysiol.2011.213769
Amann M, Sidhu SK, Weavil JC, Mangum TS, Venturelli M (2015) Autonomic responses to exercise: group III/IV muscle afferents and fatigue. Auton Neurosci 188:19–23. https://doi.org/10.1016/j.autneu.2014.10.018
Barbosa TC, Kaur J, Stephens BY, Akins JD, Keller DM, Brothers RM, Fadel PJ (2018) Attenuated forearm vascular conductance responses to rhythmic handgrip in young African-American compared with Caucasian-American men. Am J Physiol Heart Circ Physiol 315(5):H1316-h1321. https://doi.org/10.1152/ajpheart.00387.2018
Barnes WS (1980) The relationship between maximum isometric strength and intramuscular circulatory occlusion. Ergonomics 23(4):351–357. https://doi.org/10.1080/00140138008924748
Boscan P, Paton JF (2005) Excitatory convergence of periaqueductal gray and somatic afferents in the solitary tract nucleus: role for neurokinin 1 receptors. Am J Physiol Regul Integr Comp Physiol 288(1):R262-269. https://doi.org/10.1152/ajpregu.00328.2004
Butenas ALE, Rollins KS, Parr SK, Hammond ST, Ade CJ, Hageman KS, Musch TI, Copp SW (2022) Novel mechanosensory role for acid sensing ion channel subtype 1a in evoking the exercise pressor reflex in rats with heart failure. J Physiol 600(9):2105–2125. https://doi.org/10.1113/jp282923
Celie B, Boone J, Van Coster R, Bourgois J (2012) Reliability of near infrared spectroscopy (NIRS) for measuring forearm oxygenation during incremental handgrip exercise. Eur J Appl Physiol 112(6):2369–2374. https://doi.org/10.1007/s00421-011-2183-x
Chen CY, Bechtold AG, Tabor J, Bonham AC (2009) Exercise reduces GABA synaptic input onto nucleus tractus solitarii baroreceptor second-order neurons via NK1 receptor internalization in spontaneously hypertensive rats. J Neurosci 29(9):2754–2761. https://doi.org/10.1523/JNEUROSCI.4413-08.2009
Decorte N, Lafaix PA, Millet GY, Wuyam B, Verges S (2012) Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scand J Med Sci Sports 22(3):381–391. https://doi.org/10.1111/j.1600-0838.2010.01167.x
Dillon GA, Lichter ZS, Alexander LM, Vianna LC, Wang J, Fadel PJ, Greaney JL (2020) Reproducibility of the neurocardiovascular responses to common laboratory-based sympathoexcitatory stimuli in young adults. J Appl Physiol 129(5):1203–1213. https://doi.org/10.1152/japplphysiol.00210.2020
Dinenno FA, Joyner MJ (2004) Combined NO and PG inhibition augments alpha-adrenergic vasoconstriction in contracting human skeletal muscle. Am J Physiol Heart Circ Physiol 287(6):H2576–H2584
Dutra-Marques AC, Rodrigues S, Cepeda FX, Toschi-Dias E, Rondon E, Carvalho JC, Alves M, Braga A, Rondon M, Trombetta IC (2021) exaggerated exercise blood pressure as a marker of baroreflex dysfunction in normotensive metabolic syndrome patients. Front Neurosci 15:680195. https://doi.org/10.3389/fnins.2021.680195
Green AL, Wang S, Purvis S, Owen SL, Bain PG, Stein JF, Guz A, Aziz TZ, Paterson DJ (2007) Identifying cardiorespiratory neurocircuitry involved in central command during exercise in humans. J Physiol 578(Pt 2):605–612. https://doi.org/10.1113/jphysiol.2006.122549
Hureau TJ, Weavil JC, Thurston TS, Wan HY, Gifford JR, Jessop JE, Buys MJ, Richardson RS (1985) Amann M (2019) Pharmacological attenuation of group III/IV muscle afferents improves endurance performance when oxygen delivery to locomotor muscles is preserved. J Appl Physiol 127(5):1257–1266. https://doi.org/10.1152/japplphysiol.00490.2019
Lee JB, Lutz W, Omazic LJ, Jordan MA, Cacoilo J, Garland M, Power GA, Millar PJ (2021a) Blood pressure responses to static and dynamic knee extensor exercise between sexes: role of absolute contraction intensity. Med Sci Sports Exerc 53(9):1958–1968. https://doi.org/10.1249/mss.0000000000002648
Lee JB, Notay K, Seed JD, Nardone M, Omazic LJ, Millar PJ (2021b) Sex differences in muscle metaboreflex activation after static handgrip exercise. Med Sci Sports Exerc 53(12):2596–2604. https://doi.org/10.1249/mss.0000000000002747
Lee JB, Katerberg C, Bommarito J, Power GA, Millar PJ (2023) Blood pressure responses to post-exercise circulatory occlusion are attenuated following exercise-induced muscle weakness. Med Sci Sports Exerc. https://doi.org/10.1249/mss.0000000000003182
Lu Y, Ma X, Sabharwal R, Snitsarev V, Morgan D, Rahmouni K, Drummond HA, Whiteis CA, Costa V, Price M, Benson C, Welsh MJ, Chapleau MW, Abboud FM (2009) The ion channel ASIC2 is required for baroreceptor and autonomic control of the circulation. Neuron 64(6):885–897. https://doi.org/10.1016/j.neuron.2009.11.007
Luck JC, Miller AJ, Aziz F, Radtka JF 3rd, Proctor DN, Leuenberger UA, Sinoway LI, Muller MD (2017) Blood pressure and calf muscle oxygen extraction during plantar flexion exercise in peripheral artery disease. J Appl Physiol 123(1):2–10. https://doi.org/10.1152/japplphysiol.01110.2016
Matsubara T, Hayashi K, Wakatsuki K, Abe M, Ozaki N, Yamanaka A, Mizumura K, Taguchi T (2019) Thin-fibre receptors expressing acid-sensing ion channel 3 contribute to muscular mechanical hypersensitivity after exercise. Eur J Pain 23(10):1801–1813. https://doi.org/10.1002/ejp.1454
Mitchell JH, Schibye B, Payne FC III, Saltin B (1981) Response of arterial blood pressure to static exercise in relation to muscle mass, force development, and electromyographic activity. Circ Res 48(6, Suppl. I):I70–I75
Moynes J, Bentley RF, Bravo M, Kellawan JM, Tschakovsky ME (2013) Persistence of functional sympatholysis post-exercise in human skeletal muscle. Front Physiol 4:131. https://doi.org/10.3389/fphys.2013.00131
Nell HJ, Castelli LM, Bertani D, Jipson AA, Meagher SF, Melo LT, Zabjek K, Reid WD (2020) The effects of hypoxia on muscle deoxygenation and recruitment in the flexor digitorum superficialis during submaximal intermittent handgrip exercise. BMC Sports Sci Med Rehabil 12(1):16. https://doi.org/10.1186/s13102-020-00163-2
Nobrega AC, Williamson JW, Friedman DB, Araujo CG, Mitchell JH (1994) Cardiovascular responses to active and passive cycling movements. Med Sci Sports Exerc 26(6):709–714
Padley JR, Kumar NN, Li Q, Nguyen TBV, Pilowsky PM, Goodchild AK (2007) Central command regulation of circulatory function mediated by descending pontine cholinergic inputs to sympathoexcitatory rostral ventrolateral medulla neurons. Circ Res 100(2):284–291. https://doi.org/10.1161/01.RES.0000257370.63694.73
Paradis-Deschênes P, Joanisse DR, Mauriège P, Billaut F (2020) Ischemic preconditioning enhances aerobic adaptations to sprint-interval training in athletes without altering systemic hypoxic signaling and immune function. Front Sports Act Living 2:41. https://doi.org/10.3389/fspor.2020.00041
Potma EJ, van Graas IA, Stienen GJ (1995) Influence of inorganic phosphate and pH on ATP utilization in fast and slow skeletal muscle fibers. Biophys J 69(6):2580–2589. https://doi.org/10.1016/s0006-3495(95)80129-3
Potts JT (2006) Inhibitory neurotransmission in the nucleus tractus solitarii: implications for baroreflex resetting during exercise. Exp Physiol 91(1):59–72. https://doi.org/10.1113/expphysiol.2005.032227
Potts JT, Fuchs IE, Li J, Leshnower B, Mitchell JH (1999) Skeletal muscle afferent fibres release substance P in the nucleus tractus solitarii of anaesthetized cats. J Physiol 514:829–841
Queme F, Taguchi T, Mizumura K, Graven-Nielsen T (2013) Muscular heat and mechanical pain sensitivity after lengthening contractions in humans and animals. J Pain 14(11):1425–1436. https://doi.org/10.1016/j.jpain.2013.07.010
Ray CA, Monahan KD (2002) Sympathetic vascular transduction is augmented in young normotensive blacks. J Appl Physiol 92(2):651–656
Regensteiner JG, Bauer TA, Reusch JE, Quaife RA, Chen MY, Smith SC, Miller TM, Groves BM, Wolfel EE (2009) Cardiac dysfunction during exercise in uncomplicated type 2 diabetes. Med Sci Sports Exerc 41(5):977–984. https://doi.org/10.1249/MSS.0b013e3181942051
Rockenfeller R, Günther M, Stutzig N, Haeufle DFB, Siebert T, Schmitt S, Leichsenring K, Böl M, Götz T (2020) Exhaustion of skeletal muscle fibers within seconds: incorporating phosphate kinetics into a hill-type model. Front Physiol 11:306. https://doi.org/10.3389/fphys.2020.00306
Scott JA, Coombes JS, Prins JB, Leano RL, Marwick TH, Sharman JE (2008) Patients with type 2 diabetes have exaggerated brachial and central exercise blood pressure: relation to left ventricular relative wall thickness. Am J Hypertens 21(6):715–721. https://doi.org/10.1038/ajh.2008.166
Seals DR, Enoka RM (1989) Sympathetic activation is associated with increases in EMG during fatiguing exercise. J Appl Physiol 66(1):88–95
Stavres J, Sica CT, Blaha C, Herr M, Wang J, Pai S, Cauffman A, Vesek J, Yang QX, Sinoway LI (2019) The exercise pressor reflex and active O2 transport in peripheral arterial disease. Physiol Rep 7(20):e14243. https://doi.org/10.14814/phy2.14243
Stavres J, Luck JC, Ducrocq GP, Cauffman AE, Pai S, Sinoway LI (2020) Central and peripheral modulation of exercise pressor reflex sensitivity after nonfatiguing work. Am J Physiol Regul Integr Comp Physiol 319(5):R575-r583. https://doi.org/10.1152/ajpregu.00127.2020
Stavres J, Luck JC, Hamaoka T, Blaha C, Cauffman AE, Dalton P, Herr MD, Ruiz-Velasco V, Carr Z, Janicki P, Cui J (2022) A 10mg dose of amiloride increases time to failure during blood-flow-restricted plantar flexion in healthy adults without influencing blood pressure. Am J Physiol Regul Integr Comp Physiol. https://doi.org/10.1152/ajpregu.00190.2022
Stavres J, Aultman RA, Brandner CF, Newsome TQA, Vallecillo-Bustos A, Wise HL, Henderson A, Stanfield D, Mannozzi J, Graybeal AJ (2023) Hemodynamic responses to handgrip and metaboreflex activation are exaggerated in individuals with metabolic syndrome independent of resting blood pressure, waist circumference, and fasting blood glucose. Front Physiol. https://doi.org/10.3389/fphys.2023.1212775
Tschakovsky ME, Hughson RL (2003) Rapid blunting of sympathetic vasoconstriction in the human forearm at the onset of exercise. J Appl Physiol 94(5):1785–1792
Wigmore DM, Damon BM, Pober DM, Kent-Braun JA (2004) MRI measures of perfusion-related changes in human skeletal muscle during progressive contractions. J Appl Physiol 97(6):2385–2394. https://doi.org/10.1152/japplphysiol.01390.2003
Zambolin F, Giuriato G, Laginestra FG, Ottaviani MM, Favaretto T, Calabria E, Duro-Ocana P, Bagley L, Faisal A, Peçanha T, McPhee JS, Venturelli M (2022) Effects of nociceptive and mechanosensitive afferents sensitization on central and peripheral hemodynamics following exercise-induced muscle damage. J Appl Physiol 133(4):945–958. https://doi.org/10.1152/japplphysiol.00302.2022
Zambolin F, Peçanha T, Pinner S, Venturelli M, McPhee JS (2023) Effects of exercise induced muscle damage on cardiovascular responses to isometric muscle contractions and post-exercise circulatory occlusion. Eur J Appl Physiol. https://doi.org/10.1007/s00421-023-05255-8
Acknowledgements
The authors would like to thank Marshall Dearmon, Havens Lane Wise, Anabelle Vallecillo-Bustos, and Diavion Stanfield for their assistance with this study. The authors would also like to thank DeAnna Greer, Anne Speed, and Brandy Lowe for their administrative support. Lastly, the authors would like to thank all the participants who committed their time and effort to the completion of this study.
Funding
Funding was provided by Aubrey Keith and Ella Gin Lucas Endowment for Faculty Excellence and the University of Southern Mississippi.
Author information
Authors and Affiliations
Contributions
JS conceptualized the initial study idea and designed the study protocol. JS, TN, and RA collected, analyzed, and interpreted the raw data. JS prepared figures and drafted the manuscript, and all authors approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to report.
Additional information
Communicated by I. Mark Olfert.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Stavres, J., Aultman, R.S. & Newsome, T.A. Exercise pressor responses are exaggerated relative to force production during, but not following, thirty-minutes of rhythmic handgrip exercise. Eur J Appl Physiol 124, 1547–1559 (2024). https://doi.org/10.1007/s00421-023-05390-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-023-05390-2