Abstract
Purpose
This study aimed to determine the effects of hypoxia and/or blood flow restriction (BFR) on an arm-cycling repeated sprint ability test (aRSA) and its impact on elbow flexor neuromuscular function.
Methods
Fourteen volunteers performed an aRSA (10 s sprint/20 s recovery) to exhaustion in four randomized conditions: normoxia (NOR), normoxia plus BFR (NBFR), hypoxia (FiO2 = 0.13, HYP) and hypoxia plus BFR (HBFR). Maximal voluntary contraction (MVC), resting twitch force (Db10), and electromyographic responses from the elbow flexors [biceps brachii (BB)] to electrical and transcranial magnetic stimulation were obtained to assess neuromuscular function. Main effects of hypoxia, BFR, and interaction were analyzed on delta values from pre- to post-exercise.
Results
BFR and hypoxia decreased the number of sprints during aRSA with no significant cumulative effect (NOR 16 ± 8; NBFR 12 ± 4; HYP 10 ± 3 and HBFR 8 ± 3; P < 0.01). MVC decrease from pre- to post-exercise was comparable whatever the condition. M-wave amplitude (− 9.4 ± 1.9% vs. + 0.8 ± 2.0%, P < 0.01) and Db10 force (− 41.8 ± 4.7% vs. − 27.9 ± 4.5%, P < 0.01) were more altered after aRSA with BFR compared to without BFR. The exercise-induced increase in corticospinal excitability was significantly lower in hypoxic vs. normoxic conditions (e.g., BB motor evoked potential at 75% of MVC: − 2.4 ± 4.2% vs. + 16.0 ± 5.9%, respectively, P = 0.03).
Conclusion
BFR and hypoxia led to comparable aRSA performance impairments but with distinct fatigue etiology. BFR impaired the muscle excitation–contraction coupling whereas hypoxia predominantly affected corticospinal excitability indicating incapacity of the corticospinal pathway to adapt to fatigue as in normoxia.
Similar content being viewed by others
Abbreviations
- 1RM:
-
One-repetition maximum
- AMT:
-
Active motor threshold
- ANOVA:
-
Analysis of variance
- aRSA:
-
Repeated arm-cycling sprint ability test
- BB:
-
Biceps brachii
- BFR:
-
Blood flow restriction
- CMEP:
-
Cervicomedullary motor evoked potential
- CSP:
-
Cortical silent period
- EMG:
-
Electromyography
- EMS:
-
Electrical muscle stimulation
- ENS:
-
Electrical nerve stimulation
- ERT:
-
Estimated resting twitch
- ESM:
-
Electronic supplementary material
- FiO2 :
-
Fraction of inspired oxygen
- GABA:
-
Gamma-aminobutyric acid
- HBFR :
-
Hypoxia with BFR
- HYP:
-
Hypoxia
- MEP:
-
Motor evoked potential
- M max :
-
Amplitude of the muscle compound action potential
- mRNA:
-
Messenger ribonucleic acid
- MSUP :
-
Amplitude of the muscle compound action potential during maximal voluntary contraction
- MVC:
-
Maximal voluntary contraction
- M-wave:
-
Muscle compound action potential
- NBFR :
-
Normoxia with blood flow restriction
- NIRS:
-
Near-infra-red spectroscopy
- NME:
-
Neuromuscular function evaluation
- NOR:
-
Normoxia
- PFC:
-
Pre-frontal cortex
- Pmax:
-
Maximal power
- POST:
-
After repeated arm-cycling sprint ability test
- PRE:
-
Before repeated arm-cycling sprint ability test
- RMS:
-
Root mean square
- RSA:
-
Repeated sprint ability
- SD:
-
Standard deviation
- SICI:
-
Short-interval intracortical inhibition
- SIT:
-
Superimposed twitch
- SpO2 :
-
Peripheral arterial oxygen saturation
- TB:
-
Triceps brachii
- TMS:
-
Transcranial magnetic stimulation
- TSI:
-
Tissue saturation index
- TTE:
-
Time to exhaustion
- VA:
-
Voluntary activation
- VATMS :
-
Voluntary activation assessed with TMS
- η 2p :
-
Partial eta-squared
References
Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332. https://doi.org/10.1152/physrev.00015.2007
Billaut F, Buchheit M (2013) Repeated-sprint performance and vastus lateralis oxygenation: effect of limited O2 availability. Scand J Med Sci Sport 23:e185–e193. https://doi.org/10.1111/sms.12052
Billaut F, Kerris JP, Rodriguez RF et al (2013) Interaction of central and peripheral factors during repeated sprints at different levels of arterial O2 saturation. PLoS One 8:e77297. https://doi.org/10.1371/journal.pone.0077297
Bishop D, Edge J, Goodman C (2004) Muscle buffer capacity and aerobic fitness are associated with repeated-sprint ability in women. Eur J Appl Physiol 92:540–547. https://doi.org/10.1007/s00421-004-1150-1
Brandner CR, Warmington SA, Kidgell DJ (2015) Corticomotor excitability is increased following an acute bout of blood flow restriction resistance exercise. Front Hum Neurosci 9:1–10. https://doi.org/10.3389/fnhum.2015.00652
Brocherie F, Girard O, Faiss R, Millet GP (2017) Effects of repeated-sprint training in hypoxia on sea-level performance: a meta-analysis. Sport Med 47:1651–1660. https://doi.org/10.1007/s40279-017-0685-3
Calbet JAL, Rådegran G, Boushel R, Saltin B (2009) On the mechanisms that limit oxygen uptake during exercise in acute and chronic hypoxia: role of muscle mass. J Physiol 587:477–490. https://doi.org/10.1113/jphysiol.2008.162271
Calbet JAL, González-Alonso J, Helge JW et al (2015) Central and peripheral hemodynamics in exercising humans: leg vs arm exercise. Scand J Med Sci Sport 25:144–157. https://doi.org/10.1111/sms.12604
Cohen J (1988) Statistical power analysis for the behavioral sciences, 2nd edn. Lawrence Erlbaum Associates, Hillsdale, NJ
Collins BW, Pearcey GE, Buckle NCM et al (2018) Neuromuscular fatigue during repeated sprint exercise: underlying physiology and methodological considerations. Appl Physiol Nutr Metab. https://doi.org/10.1139/apnm-2018-0080
Fatela P, Reis JF, Mendonca GV et al (2016) Acute effects of exercise under different levels of blood-flow restriction on muscle activation and fatigue. Eur J Appl Physiol 116:985–995. https://doi.org/10.1007/s00421-016-3359-1
Fernandez-del-Olmo M, Rodriguez FA, Marquez G et al (2013) Isometric knee extensor fatigue following a Wingate test: peripheral and central mechanisms. Scand J Med Sci Sport 23:57–65. https://doi.org/10.1111/j.1600-0838.2011.01355.x
Forman DA, Philpott DTG, Button DC, Power KE (2015) Cadence-dependent changes in corticospinal excitability of the biceps brachii during arm cycling. J Neurophysiol 114:2285–2294. https://doi.org/10.1152/jn.00418.2015
Froyd C, Millet GY, Noakes TD (2013) The development of peripheral fatigue and short-term recovery during self-paced high-intensity exercise. J Physiol 591:1339–1346. https://doi.org/10.1113/jphysiol.2012.245316
Girard O, Mendez-Villanueva A, Bishop D (2011) Repeated-sprint ability part I: factors contributing to fatigue. Sport Med 41:673–694. https://doi.org/10.2165/11590550-000000000-00000
Girard O, Brocherie F, Millet GP (2017) Effects of altitude/hypoxia on single- and multiple-sprint performance: a comprehensive review. Sport Med 47:1931–1949. https://doi.org/10.1007/s40279-017-0733-z
Glaister M (2005) Multiple sprint work: physiological responses, mechanisms of fatigue and the influence of aerobic fitness. Sport Med 35:757–777. https://doi.org/10.2165/00007256-200535090-00003
Goodall S, Ross EZ, Romer LM (2010) Effect of graded hypoxia on supraspinal contributions to fatigue with unilateral knee-extensor contractions. J Appl Physiol 109:1842–1851. https://doi.org/10.1152/japplphysiol.00458.2010
Goods PSR, Dawson B, Landers GJ et al (2015) No additional benefit of repeat-sprint training in hypoxia than in normoxia on sea-level repeat-sprint ability. J Sports Sci Med 14:681–688
Gruet M, Temesi J, Rupp T et al (2013) Stimulation of the motor cortex and corticospinal tract to assess human muscle fatigue. Neuroscience 231:384–399. https://doi.org/10.1016/j.neuroscience.2012.10.058
Jubeau M, Rupp T, Perrey S et al (2014) Changes in voluntary activation assessed by transcranial magnetic stimulation during prolonged cycling exercise. PLoS One 9:e89157. https://doi.org/10.1371/journal.pone.0089157
Jubeau M, Rupp T, Temesi J et al (2017) Neuromuscular fatigue during prolonged exercise in hypoxia. Med Sci Sports Exerc 49:430–439. https://doi.org/10.1249/MSS.0000000000001118
Kirkendall DT (1990) Mechanisms of peripheral fatigue. Med Sci Sports Exerc 22:444–449
Koppo K, Bouckaert J, Jones AM (2002) Oxygen uptake kinetics during high-intensity arm and leg exercise. Respir Physiol Neurobiol 133:241–250. https://doi.org/10.1016/S1569-9048(02)00184-2
Loenneke JP, Fahs CA, Wilson JM, Bemben MG (2011) Blood flow restriction: the metabolite/volume threshold theory. Med Hypotheses 77:748–752. https://doi.org/10.1016/j.mehy.2011.07.029
Loenneke JP, Thiebaud RS, Abe T, Bemben MG (2014) Blood flow restriction pressure recommendations: the hormesis hypothesis. Med Hypotheses 82:623–626. https://doi.org/10.1016/j.mehy.2014.02.023
Maxwell PH (2005) Hypoxia-inducible factor as a physiological regulator. Exp Physiol 90:791–797. https://doi.org/10.1113/expphysiol.2005.030924
Mira J, Lapole T, Souron R et al (2017) Cortical voluntary activation testing methodology impacts central fatigue. Eur J Appl Physiol 117:1845–1857. https://doi.org/10.1007/s00421-017-3678-x
Pearcey GEP, Bradbury-Squires DJ, Monks M et al (2016) Arm-cycling sprints induce neuromuscular fatigue of the elbow flexors and alter corticospinal excitability of the biceps brachii. Appl Physiol Nutr Metab 41:199–209. https://doi.org/10.1139/apnm-2015-0438
Piitulainen H, Komi P, Linnamo V, Avela J (2008) Sarcolemmal excitability as investigated with M-waves after eccentric exercise in humans. J Electromyogr Kinesiol 18:672–681. https://doi.org/10.1016/j.jelekin.2007.01.004
Rothwell JC, Day BL, Thompson PD, Kujirai T (2009) Short latency intracortical inhibition: one of the most popular tools in human motor neurophysiology. J Physiol 587:11–12. https://doi.org/10.1113/jphysiol.2008.162461
Sadamoto T, Bonde-Petersen F, Suzuki Y (1983) Skeletal muscle tension, flow, pressure, and EMG during sustained isometric contractions in humans. Eur J Appl Physiol Occup Physiol 51:395–408. https://doi.org/10.1007/BF00429076
Saltin B, Rådegran G, Koskolou MD, Roach RC (1998) Skeletal muscle blood flow in humans and its regulation during exercise. Acta Physiol Scand 162:421–436. https://doi.org/10.1046/j.1365-201X.1998.0293e.x
Scott BR, Loenneke JP, Slattery KM, Dascombe BJ (2015) Exercise with blood flow restriction: an updated evidence-based approach for enhanced muscular development. Sport Med 45:313–325. https://doi.org/10.1007/s40279-014-0288-1
Shield A, Zhou S (2004) Activation with the twitch interpolation technique. Sport Med 34:253–267. https://doi.org/10.2165/00007256-200434040-00005
Smith KJ, Billaut F (2010) Influence of cerebral and muscle oxygenation on repeated-sprint ability. Eur J Appl Physiol 109:989–999. https://doi.org/10.1007/s00421-010-1444-4
Taylor CW, Ingham SA, Ferguson RA (2016) Acute and chronic effect of sprint interval training combined with postexercise blood-flow restriction in trained individuals. Exp Physiol 101:143–154. https://doi.org/10.1113/EP085293
Temesi J, Gruet M, Rupp T et al (2014) Resting and active motor thresholds versus stimulus—response curves to determine transcranial magnetic stimulation intensity in quadriceps femoris. J Neuroeng Rehabil 11:1–13. https://doi.org/10.1186/1743-0003-11-40
Thomas C (2004) Monocarboxylate transporters, blood lactate removal after supramaximal exercise, and fatigue indexes in humans. J Appl Physiol 98:804–809. https://doi.org/10.1152/japplphysiol.01057.2004
Todd G, Taylor JL, Gandevia SC (2016) Measurement of voluntary activation based on transcranial magnetic stimulation over the motor cortex. J Appl Physiol 121:678–686. https://doi.org/10.1152/japplphysiol.00293.2016
Umbel JD, Hoffman RL, Dearth DJ et al (2009) Delayed-onset muscle soreness induced by low-load blood flow-restricted exercise. Eur J Appl Physiol 107:687–695. https://doi.org/10.1007/s00421-009-1175-6
Wernbom M, Augustsson J, Thomeé R (2006) Effects of vascular occlusion on muscular endurance in dynamic knee extension exercise at different submaximal loads. J Strength Cond Res 20:372–377. https://doi.org/10.1519/R-16884.1
Wernbom M, Paulsen G, Nilsen TS et al (2012) Contractile function and sarcolemmal permeability after acute low-load resistance exercise with blood flow restriction. Eur J Appl Physiol 112:2051–2063. https://doi.org/10.1007/s00421-011-2172-0
Willis SJ, Alvarez L, Millet GP, Borrani F (2017) Changes in muscle and cerebral deoxygenation and perfusion during repeated sprints in hypoxia to exhaustion. Front Physiol 8:1–12. https://doi.org/10.3389/fphys.2017.00846
Willis SJ, Alvarez L, Borrani F, Millet GP (2018) Oxygenation time course and neuromuscular fatigue during repeated cycling sprints with bilateral blood flow restriction. Physiol Rep 6:13872. https://doi.org/10.14814/phy2.13872
Acknowledgements
Special thanks are given to the participants for their dedication, commitment, and cooperation with this study and to Naiandra Dittrich for her assistance during experimental set up and data acquisition.
Funding
Funding was provided by University Savoie Mont Blanc and the French Conseil Savoie Mont Blanc.
Author information
Authors and Affiliations
Contributions
GPM, FB, NP, and TR designed the study methodology. AP and SW collected the data and analyzed the results. AP, SW, and TR drafted the article. All authors reviewed and revised the work. All authors reviewed the final article and approved it for submission.
Corresponding author
Ethics declarations
Conflict of interest
AP was supported by a doctoral research grant from University Savoie Mont Blanc and the French Conseil Savoie Mont Blanc. The authors declare that they have no conflict of interest.
Additional information
Communicated by Guido Ferretti.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Peyrard, A., Willis, S.J., Place, N. et al. Neuromuscular evaluation of arm-cycling repeated sprints under hypoxia and/or blood flow restriction. Eur J Appl Physiol 119, 1533–1545 (2019). https://doi.org/10.1007/s00421-019-04143-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-019-04143-4