Functional reserve and sex differences during exercise to exhaustion revealed by post-exercise ischaemia and repeated supramaximal exercise.
brain oxygenation
fatigue
ischaemia
oxygen debt
oxygen deficit
oxygen extraction
performance
sex dimorphism
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
23
12
2020
accepted:
17
06
2021
pubmed:
24
6
2021
medline:
28
10
2021
entrez:
23
6
2021
Statut:
ppublish
Résumé
Females have lower fatigability than males during single limb isometric and dynamic contractions, but whether sex-differences exist during high-intensity whole-body exercise remains unknown. This study shows that males and females respond similarly to repeated supramaximal whole-body exercise, and that at task failure a large functional reserve remains in both sexes. Using post-exercise ischaemia with repeated exercise, we have shown that this functional reserve depends on the glycolytic component of substrate-level phosphorylation and is almost identical in both sexes. Metaboreflex activation during post-exercise ischaemia and the O The purpose of this study was to ascertain what mechanisms explain sex differences at task failure and to determine whether males and females have a functional reserve at exhaustion. Exercise performance, cardiorespiratory variables, oxygen deficit, and brain and muscle oxygenation were determined in 18 males and 18 females (21-36 years old) in two sessions consisting of three bouts of constant-power exercise at 120% of
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3853-3878Subventions
Organisme : Ministerio de Economía y Competitividad
ID : DEP2015-71171-R
Organisme : Ministerio de Economía y Competitividad
ID : DEP2017-86409-C2-1-P
Organisme : University of Las Palmas de Gran Canaria
ID : ULPGC 2015/05
Organisme : Agencia Canaria de Investigación, Innovación y Sociedad de la Información (ACIISI)
ID : ProID2017010106
Organisme : Natural Science and Engineering Council of Canada
ID : NSERC-15R76049
Informations de copyright
© 2021 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Allen D & Westerblad H (2004). Lactic acid-the latest performance-enhancing drug. Science 305, 1112-1113.
Allen DG, Lamb GD & Westerblad H (2008). Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88, 287-332.
Angius L, Mauger AR, Hopker J, Pascual-Leone A, Santarnecchi E & Marcora SM (2018). Bilateral extracephalic transcranial direct current stimulation improves endurance performance in healthy individuals. Brain Stimul 11, 108-117.
Ansdell P, Brownstein CG, Skarabot J, Hicks KM, Howatson G, Thomas K, Hunter SK & Goodall S (2019). Sex differences in fatigability and recovery relative to the intensity-duration relationship. J Physiol 597, 5577-5595.
Ansdell P, Thomas K, Howatson G, Hunter S & Goodall S (2017). Contraction intensity and sex differences in knee-extensor fatigability. J Electromyogr Kinesiol 37, 68-74.
Bangsbo J, Gollnick PD, Graham TE, Juel C, Kiens B, Mizuno M & Saltin B (1990). Anaerobic energy production and O2 deficit-debt relationship during exhaustive exercise in humans. J Physiol 422, 539-559.
Barclay CJ (1996). Mechanical efficiency and fatigue of fast and slow muscles of the mouse. J Physiol 497 781-794.
Black MI, Jones AM, Blackwell JR, Bailey SJ, Wylie LJ, McDonagh ST, Thompson C, Kelly J, Sumners P, Mileva KN, Bowtell JL & Vanhatalo A (2017). Muscle metabolic and neuromuscular determinants of fatigue during cycling in different exercise intensity domains. J Appl Physiol 122, 446-459.
Blei ML, Conley KE & Kushmerick MJ (1993). Separate measures of ATP utilization and recovery in human skeletal muscle. J Physiol 465, 203-222.
Botcazou M, Gratas-Delamarche A, Allain S, Jacob C, Bentue-Ferrer D, Delamarche P & Zouhal H (2006). Influence of menstrual cycle phase on catecholamine response to sprint exercise in the woman. Appl Physiol Nutr Metab 31, 604-611.
Boushel R, Langberg H, Olesen J, Gonzales-Alonzo J, Bulow J & Kjaer M (2001). Monitoring tissue oxygen availability with near infrared spectroscopy (NIRS) in health and disease. Scand J Med Sci Sports 11, 213-222.
Brandner CR, Warmington SA & Kidgell DJ (2015). Corticomotor excitability is increased following an acute bout of blood flow restriction resistance exercise. Front Hum Neurosci 9, 652.
Bruton JD, Place N, Yamada T, Silva JP, Andrade FH, Dahlstedt AJ, Zhang SJ, Katz A, Larsson NG & Westerblad H (2008). Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 overexpressing mice. J Physiol 586, 175-184.
Bushman B, Masterson G & Nelsen J (2006). Anaerobic power performance and the menstrual cycle: eumenorrheic and oral contraceptive users. J Sports Med Phys Fitness 46, 132-137.
Cady EB, Jones DA, Lynn J & Newham DJ (1989). Changes in force and intracellular metabolites during fatigue of human skeletal muscle. J Physiol 418, 311-325.
Calbet JAL, Chavarren J & Dorado C (1997). Fractional use of anaerobic capacity during a 30- and a 45-s Wingate test. Eur J Appl Physiol 76, 308-313.
Calbet JAL, Losa-Reyna J, Torres-Peralta R, Rasmussen P, Ponce-Gonzalez JG, Sheel AW, de la Calle-Herrero J, Guadalupe-Grau A, Morales-Alamo D, Fuentes T, Rodriguez-Garcia L, Siebenmann C, Boushel R & Lundby C (2015). Limitations to oxygen transport and utilization during sprint exercise in humans: evidence for a functional reserve in muscle O2 diffusing capacity. J Physiol 593, 4649-4664.
Calbet JAL, Martin-Rodriguez S, Martin-Rincon M & Morales-Alamo D (2020). An integrative approach to the regulation of mitochondrial respiration during exercise: Focus on high-intensity exercise. Redox Biol 35, 101478.
Calbet JAL, Moysi JS, Dorado C & Rodriguez LP (1998). Bone mineral content and density in professional tennis players. Calcif Tissue Int 62, 491-496.
Cardinale DA, Larsen FJ, Jensen-Urstad M, Rullman E, Sondergaard H, Morales-Alamo D, Ekblom B, Calbet JAL & Boushel R (2019). Muscle mass and inspired oxygen influence oxygen extraction at maximal exercise: Role of mitochondrial oxygen affinity. Acta Physiol 225, e13110.
Cardinale DA, Larsen FJ, Schiffer TA, Morales-Alamo D, Ekblom B, Calbet JAL, Holmberg HC & Boushel R (2018). Superior intrinsic mitochondrial respiration in women than in men. Front Physiol 9, 1133.
Coelho AC, Cannon DT, Cao R, Porszasz J, Casaburi R, Knorst MM & Rossiter HB (2015). Instantaneous quantification of skeletal muscle activation, power production, and fatigue during cycle ergometry. J Appl Physiol 118, 646-654.
Copithorne DB, Rice CL & McNeil CJ (2020). Effect of blood flow occlusion on corticospinal excitability during sustained low-intensity isometric elbow flexion. J Neurophysiol 123, 1113-1119.
Coupland ME, Puchert E & Ranatunga KW (2001). Temperature dependence of active tension in mammalian (rabbit psoas) muscle fibres: effect of inorganic phosphate. J Physiol 536, 879-891.
Curtelin D, Morales-Alamo D, Torres-Peralta R, Rasmussen P, Martin-Rincon M, Perez-Valera M, Siebenmann C, Perez-Suarez I, Cherouveim E, Sheel AW, Lundby C & Calbet JA (2018). Cerebral blood flow, frontal lobe oxygenation and intra-arterial blood pressure during sprint exercise in normoxia and severe acute hypoxia in humans. J Cereb Blood Flow Metab 38, 136-150.
Edgell H & Stickland MK (2014). Activation of the carotid chemoreflex secondary to muscle metaboreflex stimulation in men. Am J Physiol Regul Integr Comp Physiol 306, R693-R700.
Esbjornsson Liljedahl M, Holm I, Sylven C & Jansson E (1996). Different responses of skeletal muscle following sprint training in men and women. Eur J Appl Physiol Occup Physiol 74, 375-383.
Esbjornsson-Liljedahl M, Bodin K & Jansson E (2002). Smaller muscle ATP reduction in women than in men by repeated bouts of sprint exercise. J Appl Physiol 93, 1075-1083.
Ferreira JJ, Pequera G, Launikonis BS, Rios E & Brum G (2021). A chloride channel blocker prevents the suppression by inorganic phosphate of the cytosolic calcium signals that control muscle contraction. J Physiol 599, 157-170.
Fitts RH (1994). Cellular mechanisms of muscle fatigue. Physiol Rev 74, 49-94.
Fryer MW, Owen VJ, Lamb GD & Stephenson DG (1995). Effects of creatine phosphate and Pi on Ca2+ movements and tension development in rat skinned skeletal muscle fibres. J Physiol 482 123-140.
Gaitanos GC, Williams C, Boobis LH & Brooks S (1993). Human muscle metabolism during intermittent maximal exercise. J Appl Physiol 75, 712-719.
Gandevia SC (2001). Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81, 1725-1789.
Gastin PB, Costill DL, Lawson DL, Krzeminski K & McConell GK (1995). Accumulated oxygen deficit during supramaximal all-out and constant intensity exercise. Med Sci Sports Exerc 27, 255-263.
Gejl KD, Hvid LG, Frandsen U, Jensen K, Sahlin K & Ortenblad N (2014). Muscle glycogen content modifies SR Ca2+ release rate in elite endurance athletes. Med Sci Sports Exerc 46, 496-505.
Gelabert-Rebato M, Martin-Rincon M, Galvan-Alvarez V, Gallego-Selles A, Martinez-Canton M, Vega-Morales T, Wiebe JC, Fernandez-Del CC, Castilla-Hernandez E, Diaz-Tiberio O & Calbet JAL (2019a). A single dose of the mango leaf extract Zynamite® in combination with quercetin enhances peak power output during repeated sprint exercise in men and women. Nutrients 11, 2592.
Gelabert-Rebato M, Wiebe JC, Martin-Rincon M, Galvan-Alvarez V, Curtelin D, Perez-Valera M, Habib JJ, Pérez-López A, Vega T, Morales-Alamo D & Calbet JAL (2019b). Enhancement of exercise performance by 48 hours, and 15-day supplementation with mangiferin and luteolin in men. Nutrients 11, 344.
Gelabert-Rebato M, Wiebe JC, Martin-Rincon M, Gericke N, Perez-Valera M, Curtelin D, Galvan-Alvarez V, Lopez-Rios L, Morales-Alamo D & Calbet JAL (2018). Mangifera indica L. leaf extract in combination with luteolin or quercetin enhances VO2peak and peak power output, and preserves skeletal muscle function during ischemia-reperfusion in humans. Front Physiol 9, 740.
Green HJ, Fraser IG & Ranney DA (1984). Male and female differences in enzyme activities of energy metabolism in vastus lateralis muscle. J Neurol Sci 65, 323-331.
Hagberg JM, Coyle EF, Carroll JE, Miller JM, Martin WH & Brooke MH. (1982). Exercise hyperventilation in patients with McArdle’s disease. J Appl Physiol 52, 991-994.
Harris RC, Edwards RH, Hultman E, Nordesjo LO, Nylind B & Sahlin K (1976). The time course of phosphorylcreatine resynthesis during recovery of the quadriceps muscle in man. Pflugers Arch 367, 137-142.
Harris RC, Hultman E, Kaijser L & Nordesjo LO (1975). The effect of circulatory occlusion on isometric exercise capacity and energy metabolism of the quadriceps muscle in man. Scand J Clin Lab Invest 35, 87-95.
Heidari S, Babor TF, De Castro P, Tort S & Curno M (2016). Sex and gender equity in research: rationale for the SAGER guidelines and recommended use. Res Integr Peer Rev 1, 2.
Heinonen I, Duncker DJ, Knuuti J & Kalliokoski KK (2012). The effect of acute exercise with increasing workloads on inactive muscle blood flow and its heterogeneity in humans. Eur J Appl Physiol 112, 3503-3509,
Hill DW & Vingren JL (2014). Effects of exercise mode and participant sex on measures of anaerobic capacity. J Sports Med Phys Fitness 54, 255-263.
Hinkle PC, Kumar MA, Resetar A & Harris DL (1991). Mechanistic stoichiometry of mitochondrial oxidative phosphorylation. Biochemistry 30, 3576-3582.
Hinks A, MacDougall KB, Mashouri P & Smith IC (2021). Can a chloride channel blocker mitigate muscle fatigue? J Physiol 599, 2145-2147.
Hunter SK (2014). Sex differences in human fatigability: mechanisms and insight to physiological responses. Acta Physiol 210, 768-789.
Hunter SK (2016a). The relevance of sex differences in performance fatigability. Med Sci Sports Exerc 48, 2247-2256.
Hunter SK (2016b). Sex differences in fatigability of dynamic contractions. Exp Physiol 101, 250-255.
Hureau TJ, Weavil JC, Thurston TS, Wan HY, Gifford JR, Jessop JE, Buys MJ, Richardson RS & 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, 1257-1266.
Jacobs I, Tesch PA, Bar-Or O, Karlsson J & Dotan R (1983). Lactate in human skeletal muscle after 10 and 30 s of supramaximal exercise. J Appl Physiol 55, 365-367.
Jarvis SS, VanGundy TB, Galbreath MM, Shibata S, Okazaki K, Reelick MF, Levine BD & Fu Q (2011). Sex differences in the modulation of vasomotor sympathetic outflow during static handgrip exercise in healthy young humans. Am J Physiol Regul Integr Comp Physiol 301, R193-R200.
Jaworowski A, Porter MM, Holmback AM, Downham D & Lexell J (2002). Enzyme activities in the tibialis anterior muscle of young moderately active men and women: relationship with body composition, muscle cross-sectional area and fibre type composition. Acta Physiol Scand 176, 215-225.
Jensen R, Nielsen J & Ortenblad N (2020). Inhibition of glycogenolysis prolongs action potential repriming period and impairs muscle function in rat skeletal muscle. J Physiol 598, 789-803.
Joshi H & Edgell H (2019). Sex differences in the ventilatory and cardiovascular response to supine and tilted metaboreflex activation. Physiol Rep 7, e14041.
Jubrias SA, Crowther GJ, Shankland EG, Gronka RK & Conley KE (2003). Acidosis inhibits oxidative phosphorylation in contracting human skeletal muscle in vivo. J Physiol 553, 589-599.
Jubrias SA, Vollestad NK, Gronka RK & Kushmerick MJ (2008). Contraction coupling efficiency of human first dorsal interosseous muscle. J Physiol 586, 1993-2002.
Kayser B (2003). Exercise starts and ends in the brain. Eur J Appl Physiol 90, 411-419.
Lam E, Greenhough E, Nazari P, White MJ & Bruce RM (2019). Muscle metaboreflex activation increases ventilation and heart rate during dynamic exercise in humans. Exp Physiol 104, 1472-1481.
Larsen FJ, Schiffer TA, Ortenblad N, Zinner C, Morales-Alamo D, Willis SJ, Calbet JA, Holmberg H-C & Boushel R (2016). High-intensity sprint training inhibits mitochondrial respiration through aconitase inactivation. FASEB J 30, 417-427.
Loe H, Rognmo O, Saltin B & Wisloff U (2013). Aerobic capacity reference data in 3816 healthy men and women 20-90 years. PLoS One 8, e64319.
Marcora S (2010). Counterpoint: Afferent feedback from fatigued locomotor muscles is not an important determinant of endurance exercise performance. J Appl Physiol 108, 454-456; discussion 456-457.
Marcora SM & Staiano W (2010). The limit to exercise tolerance in humans: mind over muscle? Eur J Appl Physiol 109, 763-770.
Martin-Rincon M, Gonzalez-Henriquez JJ, Losa-Reyna J, Perez-Suarez I, Ponce-Gonzalez JG, de La Calle-Herrero J, Perez-Valera M, Perez-Lopez A, Curtelin D, Cherouveim ED, Morales-Alamo D & Calbet JAL (2019). Impact of data averaging strategies on VO2max assessment: Mathematical modeling and reliability. Scand J Med Sci Sports 29, 1473-1488.
Mattu AT, Iannetta D, MacInnis MJ, Doyle-Baker PK & Murias JM (2020). Menstrual and oral contraceptive cycle phases do not affect submaximal and maximal exercise responses. Scand J Med Sci Sports 30, 472-484.
Medbo JI & Burgers S (1990). Effect of training on the anaerobic capacity. Med Sci Sports Exerc 22, 501-507.
Medbo JI, Mohn AC, Tabata I, Bahr R, Vaage O & Sejersted OM (1988). Anaerobic capacity determined by maximal accumulated O2 deficit. J Appl Physiol 64, 50-60.
Medbo JI & Tabata I (1989). Relative importance of aerobic and anaerobic energy release during short-lasting exhausting bicycle exercise. J Appl Physiol 67, 1881-1886.
Medbo JI & Tabata I (1993). Anaerobic energy release in working muscle during 30 s to 3 min of exhausting bicycling. J Appl Physiol 75, 1654-1660.
Morales-Alamo D & Calbet JA (2014). Free radicals and sprint exercise in humans. Free Radic Res 48, 30-42.
Morales-Alamo D, Losa-Reyna J, Torres-Peralta R, Martin-Rincon M, Perez-Valera M, Curtelin D, Ponce-Gonzalez JG, Santana A & Calbet JA (2015). What limits performance during whole-body incremental exercise to exhaustion in humans? J Physiol 593, 4631-4648.
Myburgh KH (2004). Can any metabolites partially alleviate fatigue manifestations at the cross-bridge? Med Sci Sports Exerc 36, 20-27.
Parolin ML, Chesley A, Matsos MP, Spriet LL, Jones NL & Heigenhauser GJ (1999). Regulation of skeletal muscle glycogen phosphorylase and PDH during maximal intermittent exercise. Am J Physiol 277, E890-E900.
Pedersen TH, Clausen T & Nielsen OB (2003). Loss of force induced by high extracellular [K+] in rat muscle: effect of temperature, lactic acid and β2-agonist. J Physiol 551, 277-286.
Perez-Gomez J, Rodriguez GV, Ara I, Olmedillas H, Chavarren J, Gonzalez-Henriquez JJ, Dorado C & Calbet JA (2008). Role of muscle mass on sprint performance: gender differences? Eur J Appl Physiol 102, 685-694.
Perez-Suarez I, Martin-Rincon M, Gonzalez-Henriquez JJ, Fezzardi C, Perez-Regalado S, Galvan-Alvarez V, Juan-Habib JW, Morales-Alamo D & Calbet JAL (2018). Accuracy and precision of the COSMED K5 portable analyser. Front Physiol 9, 1764.
Poole DC & Jones AM (2012). Oxygen uptake kinetics. Compr Physiol 2, 933-996.
Poole DC & Jones AM (2017). Measurement of the maximum oxygen uptake VO2max: VO2peak is no longer acceptable. J Appl Physiol 122, 997-1002.
Quaresima V & Ferrari M (2009). Muscle oxygenation by near-infrared-based tissue oximeters. J Appl Physiol 107, 371; author reply 372-373.
Quistorff B, Johansen L & Sahlin K (1993). Absence of phosphocreatine resynthesis in human calf muscle during ischaemic recovery. Biochem J 291 681-686.
Ramsbottom R, Nevill ME, Nevill AM & Hazeldine R (1997). Accumulated oxygen deficit and shuttle run performance in physically active men and women. J Sports Sci 15, 207-214.
Richardson RS, Noyszewski EA, Kendrick KF, Leigh JS & Wagner PD (1995). Myoglobin O2 desaturation during exercise. Evidence of limited O2 transport. J Clin Invest 96, 1916-1926.
Sahlin K & Harris RC (2011). The creatine kinase reaction: a simple reaction with functional complexity. Amino Acids 40, 1363-1367.
Sahlin K & Ren JM (1989). Relationship of contraction capacity to metabolic changes during recovery from a fatiguing contraction. J Appl Physiol 67, 648-654.
Samora M, Teixeira AL, Sabino-Carvalho JL & Vianna LC (2019). Spontaneous cardiac baroreflex sensitivity is enhanced during post-exercise ischemia in men but not in women. Eur J Appl Physiol 119, 103-111.
Sander M, Macefield VG & Henderson LA (2010). Cortical and brain stem changes in neural activity during static handgrip and postexercise ischemia in humans. J Appl Physiol 108, 1691-1700.
Senefeld J, Pereira HM, Elliott N, Yoon T & Hunter SK (2018). Sex differences in mechanisms of recovery after isometric and dynamic fatiguing tasks. Med Sci Sports Exerc 50, 1070-1083.
Shaharudin S, Ghosh AK & Ismail AA (2011). Anaerobic capacity of physically active eumenorrheic females at mid-luteal and mid-follicular phases of ovarian cycle. J Sports Med Phys Fitness 51, 576-582.
Sidhu SK, Weavil JC, Mangum TS, Jessop JE, Richardson RS, Morgan DE & Amann M (2017). Group III/IV locomotor muscle afferents alter motor cortical and corticospinal excitability and promote central fatigue during cycling exercise. Clin Neurophysiol 128, 44-55.
Sidhu SK, Weavil JC, Venturelli M, Garten RS, Rossman MJ, Richardson RS, Gmelch BS, Morgan DE & Amann M (2014). Spinal μ-opioid receptor-sensitive lower limb muscle afferents determine corticospinal responsiveness and promote central fatigue in upper limb muscle. J Physiol 592, 5011-5024.
Simoneau JA & Bouchard C (1989). Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am J Physiol 257, E567-E572.
Thomas K, Elmeua M, Howatson G & Goodall S (2016). Intensity-dependent contribution of neuromuscular fatigue after constant-load cycling. Med Sci Sports Exerc 48, 1751-1760.
Torres-Peralta R, Morales-Alamo D, Gonzalez-Izal M, Losa-Reyna J, Perez-Suarez I, Izquierdo M & Calbet JA (2016). Task failure during exercise to exhaustion in normoxia and hypoxia is due to reduced muscle activation caused by central mechanisms while muscle metaboreflex does not limit performance. Front Physiol 6, 414.
van der Zee P, Cope M, Arridge SR, Essenpreis M, Potter LA, Edwards AD, Wyatt JS, McCormick DC, Roth SC & Reynolds EO, et al. (1992). Experimentally measured optical pathlengths for the adult head, calf and forearm and the head of the newborn infant as a function of inter optode spacing. Adv Exp Med Biol 316, 143-153.
Wan HY, Weavil JC, Thurston TS, Georgescu VP, Hureau TJ, Bledsoe AD, Buys MJ, Jessop JE, Richardson RS & Amann M (2020). The exercise pressor reflex and chemoreflex interaction: cardiovascular implications for the exercising human. J Physiol 598, 2311-2321.
Welch JF, Archiza B, Guenette JA, West CR & Sheel AW (2018). Sex differences in diaphragmatic fatigue: the cardiovascular response to inspiratory resistance. J Physiol 596, 4017-4032.
Westerblad H & Allen DG (2011). Emerging roles of ROS/RNS in muscle function and fatigue. Antioxid Redox Signal 15, 2487-2499.
Westerblad H, Bruton JD & Lannergren J (1997). The effect of intracellular pH on contractile function of intact, single fibres of mouse muscle declines with increasing temperature. J Physiol 500, 193-204.
Weyand PG, Cureton KJ, Conley DS & Higbie EJ (1993). Peak oxygen deficit during one- and two-legged cycling in men and women. Med Sci Sports Exerc 25, 584-591.
Woledge RC (1998). Possible effects of fatigue on muscle efficiency. Acta Physiol Scand 162, 267-273.
Yoon T, Schlinder DB, Griffith EE & Hunter SK (2007). Mechanisms of fatigue differ after low- and high-force fatiguing contractions in men and women. Muscle Nerve 36, 515-524.