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Sex differences in neuromuscular function after repeated eccentric contractions of the knee extensor muscles

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Abstract

Purpose

This study examined the mechanisms for force and power reduction during and up to 48 h after maximal eccentric contractions of the knee extensor muscles in young men and women.

Methods

13 men (22.8 ± 2.6 years) and 13 women (21.6 ± 2.2 years) performed 150 maximal effort eccentric contractions (5 sets of 30) with the knee extensor muscles at 60° s−1. Maximal voluntary isometric contractions (MVIC) and maximal voluntary concentric contractions (MVCC) were performed before and after the 150 eccentric contractions. The MVCCs involved a set of two isokinetic contractions at 60° s−1 and sets of isotonic contractions performed at seven different resistance loads (1 N m, 10, 20, 30, 40, 50, and 60% MVIC). Electrical stimulation was used during the MVICs and at rest to determine changes in voluntary activation and contractile properties.

Results

At baseline, men were stronger than women (MVIC: 276 ± 48 vs. 133 ± 37 N m) and more powerful (MVCC: 649 ± 77 vs. 346 ± 78 W). At termination of the eccentric contractions, voluntary activation, resting twitch amplitude, and peak power during concentric contractions at the seven loads and at 60° s−1 decreased (P < 0.05) similarly in the men and women. At 48 h post-exercise, the MVIC torque, power (for loads ≥20–60% MVIC), and voluntary activation remained depressed (P < 0.05), but the resting twitch had returned to baseline (P > 0.05) with no sex differences.

Conclusion

Central mechanisms were primarily responsible for the depressed maximal force production up to 48 h after repeated eccentric contractions of the knee extensors and these mechanisms were similar in men and women.

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Abbreviations

ANOVA:

Analysis of variance

EMG:

Electromyography

MVCC:

Maximal voluntary concentric contraction

MVIC:

Maximal voluntary isometric contraction

RT:

Resting twitch

RMS:

Root mean square

VA:

Voluntary activation

References

  • Allen D (2001) Eccentric muscle damage: mechanisms of early reduction of force. Acta Physiol Scand 171(3):311–319

    Article  CAS  PubMed  Google Scholar 

  • Avin KG, Naughton MR, Ford BW, Moore HE, Monitto-Webber MN, Stark AM, Gentile AJ, Law LA (2010) Sex differences in fatigue resistance are muscle group dependent. Med Sci Sports Exerc 42(10):1943–1950

    Article  PubMed  PubMed Central  Google Scholar 

  • Bampouras TM, Reeves ND, Baltzopoulos V, Maganaris CN (2006) Muscle activation assessment: effects of method, stimulus number, and joint angle. Muscle Nerve 34(6):740–746. doi:10.1002/mus.20610

    Article  PubMed  Google Scholar 

  • Bigland-Ritchie B, Johansson R, Lippold OC, Woods JJ (1983) Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J Neurophysiol 50(1):313–324

    CAS  PubMed  Google Scholar 

  • Billaut F, Bishop DJ (2012) Mechanical work accounts for sex differences in fatigue during repeated sprints. Eur J Appl Physiol 112(4):1429–1436. doi:10.1007/s00421-011-2110-1

    Article  PubMed  Google Scholar 

  • Borg GA (1982) Psychophysical bases of perceived exertion. Med Sci Sports Exerc 14(5):377–381

    Article  CAS  PubMed  Google Scholar 

  • Borsa PA, Sauers EL (2000) The importance of gender on myokinetic deficits before and after microinjury. Med Sci Sports Exerc 32(5):891–896

    Article  CAS  PubMed  Google Scholar 

  • Byrne C, Twist C, Eston R (2004) Neuromuscular function after exercise-induced muscle damage. Sports Med 34(1):49–69

    Article  PubMed  Google Scholar 

  • Campenella B, Mattacola CG, Kimura IF (2000) Effect of visual feedback and verbal encouragement on concentric quadriceps and hamstrings peak torque of males and females. Isokinet Exerc Sci 8(1):1–6

    Google Scholar 

  • Clark BC, Collier SR, Manini TM, Ploutz-Snyder LL (2005) Sex differences in muscle fatigability and activation patterns of the human quadriceps femoris. Eur J Appl Physiol 94(1–2):196–206

    Article  PubMed  Google Scholar 

  • Coratella G, Bellin G, Beato M, Schena F (2015) Fatigue affects peak joint torque angle in hamstrings but not in quadriceps. J Sports Sci 33(12):1276–1282. doi:10.1080/02640414.2014.986185

    Article  PubMed  Google Scholar 

  • De Ruiter C, Kooistra R, Paalman M, De Haan A (2004) Initial phase of maximal voluntary and electrically stimulated knee extension torque development at different knee angles. J Appl Physiol 97(5):1693–1701

    Article  PubMed  Google Scholar 

  • Doguet V, Jubeau M, Dorel S, Couturier A, Lacourpaille L, Guevel A, Guilhem G (2016) Time-course of neuromuscular changes during and after maximal eccentric contractions. Front Physiol 7:137. doi:10.3389/fphys.2016.00137

    Article  PubMed  PubMed Central  Google Scholar 

  • Enoka RM, Duchateau J (2008) Muscle fatigue: what, why and how it influences muscle function. J Physiol 586(1):11–23

    Article  CAS  PubMed  Google Scholar 

  • Farina D, Merletti R, Enoka RM (2004) The extraction of neural strategies from the surface EMG. J Appl Physiol 96:1486–1496

    Article  PubMed  Google Scholar 

  • Farina D, Merletti R, Enoka RM (2014) The extraction of neural strategies from the surface EMG: an update. J Appl Physiol (1985) 117 (11):1215–1230. doi:10.1152/japplphysiol.00162.2014

    Article  PubMed  PubMed Central  Google Scholar 

  • Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81(4):1725–1789

    CAS  PubMed  Google Scholar 

  • Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10(5):361–374

    Article  CAS  PubMed  Google Scholar 

  • Hicks KM, Onambele GL, Winwood K, Morse CI (2016) Muscle damage following maximal eccentric knee extensions in males and females. PLoS One 11(3):e0150848. doi:10.1371/journal.pone.0150848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubal MJ, Rubinstein SR, Clarkson PM (2008) Muscle function in men and women during maximal eccentric exercise. J Strength Cond Res Natl Strength Cond Assoc 22(4):1332–1338. doi:10.1519/JSC.0b013e31817392ec

    Article  Google Scholar 

  • Hunter SK (2014) Sex differences in human fatigability: mechanisms and insight to physiological responses. Acta Physiol (Oxf) 210(4):768–789. doi:10.1111/apha.12234

    Article  CAS  PubMed Central  Google Scholar 

  • Hunter SK (2016a) The relevance of sex differences in performance fatigability. Med Sci Sports Exerc 48(11):2247–2256. doi:10.1249/mss.0000000000000928

    Article  PubMed  Google Scholar 

  • Hunter SK (2016b) Sex differences in fatigability of dynamic contractions. Exp Physiol 101(2):250–255. doi:10.1113/ep085370

    Article  PubMed  Google Scholar 

  • Hunter SK, Enoka RM (2001) Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions. J Appl Physiol 91(6):2686–2694

    CAS  PubMed  Google Scholar 

  • Hunter SK, Critchlow A, Shin IS, Enoka RM (2004) Fatigability of the elbow flexor muscles for a sustained submaximal contraction is similar in men and women matched for strength. J Appl Physiol 96:195–202

    Article  PubMed  Google Scholar 

  • Kellis E, Baltzopoulos V (1996) Resistive eccentric exercise: effects of visual feedback on maximum moment of knee extensors and flexors. J Orthop Sports Phys Therapy 23(2):120–124

    Article  CAS  Google Scholar 

  • Kennedy DS, Fitzpatrick SC, Gandevia SC, Taylor JL (2015) Fatigue-related firing of muscle nociceptors reduces voluntary activation of ipsilateral but not contralateral lower limb muscles. J Appl Physiol (1985) 118 (4):408–418. doi:10.1152/japplphysiol.00375.2014

    Article  Google Scholar 

  • Kriska AM, Bennett PH (1992) An epidemiological perspective of the relationship between physical activity and NIDDM: from activity assessment to intervention. Diabetes Metab Rev 8(4):355–372

    Article  CAS  PubMed  Google Scholar 

  • LaStayo PC, Woolf JM, Lewek MD, Snyder-Mackler L, Reich T, Lindstedt SL (2003) Eccentric muscle contractions: their contribution to injury, prevention, rehabilitation, and sport. J Orthop Sports Phys Ther 33(10):557–571. doi:10.2519/jospt.2003.33.10.557

    Article  PubMed  Google Scholar 

  • LaStayo P, Marcus R, Dibble L, Frajacomo F, Lindstedt S (2014) Eccentric exercise in rehabilitation: safety, feasibility, and application. J Appl Physiol 116(11):1426–1434

    Article  PubMed  Google Scholar 

  • Lau WY, Blazevich AJ, Newton MJ, Wu SSX, Nosaka K (2015) Assessment of muscle pain induced by elbow-flexor eccentric exercise. J Athl Train 50(11):1140–1148

    Article  PubMed  PubMed Central  Google Scholar 

  • Le Pera D, Graven-Nielsen T, Valeriani M, Oliviero A, Di Lazzaro V, Tonali PA, Arendt-Nielsen L (2001) Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clin Neurophysiol 112(9):1633–1641

    Article  CAS  PubMed  Google Scholar 

  • Lindstedt SL, LaStayo PC, Reich TE (2001) When active muscles lengthen: properties and consequences of eccentric contractions. Physiology 16(6):256–261

    CAS  Google Scholar 

  • Martin PG, Rattey J (2007) Central fatigue explains sex differences in muscle fatigue and contralateral cross-over effects of maximal contractions. Pflugers Arch 454(6):957–969

    Article  CAS  PubMed  Google Scholar 

  • Martin V, Millet GY, Lattier G, Perrod L (2004) Effects of recovery modes after knee extensor muscles eccentric contractions. Med Sci Sports Exerc 36(11):1907–1915

    Article  PubMed  Google Scholar 

  • Minahan C, Joyce S, Bulmer AC, Cronin N, Sabapathy S (2015) The influence of estradiol on muscle damage and leg strength after intense eccentric exercise. Eur J Appl Physiol 115(7):1493–1500. doi:10.1007/s00421-015-3133-9

    Article  CAS  PubMed  Google Scholar 

  • Nishikawa K (2016) Eccentric contraction: unraveling mechanisms of force enhancement and energy conservation. J Exp Biol 219(Pt 2):189–196. doi:10.1242/jeb.124057

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  • Pietrosimone BG, Selkow NM, Ingersoll CD, Hart JM, Saliba SA (2011) Electrode type and placement configuration for quadriceps activation evaluation. J Athl Train 46(6):621

    Article  PubMed  PubMed Central  Google Scholar 

  • Pincivero DM, Gear WS, Sterner RL, Karunakara RG (2000) Gender differences in the relationship between quadriceps work and fatigue during high-intensity exercise. J Strength Cond Res 14(2):202–206

    Google Scholar 

  • Power GA, Dalton BH, Rice CL, Vandervoort AA (2010) Delayed recovery of velocity-dependent power loss following eccentric actions of the ankle dorsiflexors. J Appl Physiol 109(3):669–676. doi:10.1152/japplphysiol.01254.2009

    Article  PubMed  PubMed Central  Google Scholar 

  • Power GA, Dalton BH, Rice CL, Vandervoort AA (2011) Reproducibility of velocity-dependent power: before and after lengthening contractions. Appl Physiol Nutr Metab 36(5):626–633

    Article  PubMed  Google Scholar 

  • Power GA, Dalton BH, Rice CL, Vandervoort AA (2013) Peak power is reduced following lengthening contractions despite a maintenance of shortening velocity. Appl Physiol Nutr Metab 38 (12):1196–1205. doi:10.1139/apnm-2013-0092

    Article  PubMed  Google Scholar 

  • Prasartwuth O, Taylor JL, Gandevia SC (2005) Maximal force, voluntary activation and muscle soreness after eccentric damage to human elbow flexor muscles. J Physiol 567(Pt 1):337–348. doi:10.1113/jphysiol.2005.087767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Racinais S, Bringard A, Puchaux K, Noakes TD, Perrey S (2008) Modulation in voluntary neural drive in relation to muscle soreness. Eur J Appl Physiol 102(4):439–446. doi:10.1007/s00421-007-0604-7

    Article  CAS  PubMed  Google Scholar 

  • Rinard J, Clarkson PM, Smith LL, Grossman M (2000) Response of males and females to high-force eccentric exercise. J Sports Sci 18(4):229–236. doi:10.1080/026404100364965

    Article  CAS  PubMed  Google Scholar 

  • Russ DW, Kent-Braun JA (2003) Sex differences in human skeletal muscle fatigue are eliminated under ischemic conditions. J Appl Physiol 94(6):2414–2422

    Article  PubMed  Google Scholar 

  • Sayers SP, Clarkson PM (2001) Force recovery after eccentric exercise in males and females. Eur J Appl Physiol 84(1–2):122–126

    Article  CAS  PubMed  Google Scholar 

  • Sayers SP, Clarkson PM, Rouzier PA, Kamen G (1999) Adverse events associated with eccentric exercise protocols: six case studies. Med Sci Sports Exerc 31(12):1697–1702

    Article  CAS  PubMed  Google Scholar 

  • Sewright KA, Hubal MJ, Kearns A, Holbrook MT, Clarkson PM (2008) Sex differences in response to maximal eccentric exercise. Med Sci Sports Exerc 40(2):242–251

    Article  PubMed  Google Scholar 

  • Suter E, Herzog W (2001) Effect of number of stimuli and timing of twitch application on variability in interpolated twitch torque. J Appl Physiol (1985) 90(3):1036–1040

    CAS  Google Scholar 

  • Wust RC, Morse CI, de Haan A, Jones DA, Degens H (2008) Sex differences in contractile properties and fatigue resistance of human skeletal muscle. Exp Physiol 93(7):843–850

    Article  PubMed  Google Scholar 

  • Yoon T, Schlinder Delap B, Griffith EE, Hunter SK (2007) Mechanisms of fatigue differ after low- and high-force fatiguing contractions in men and women. Muscle Nerve 36(4):515–524. doi:10.1002/mus.20844

    Article  PubMed  Google Scholar 

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Acknowledgements

Michigan Technological University start-up fund to TY. Thank you to Dr. Elmer for helping to review the manuscript and provide helpful suggestions.

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Authors and Affiliations

  1. Department of Kinesiology and Integrative Physiology, Michigan Technological University, 1400 Townsend Drive, Houghton, MI, USA

    Claire Eischer, Matt Gage & Tejin Yoon

  2. Department of Physical Therapy, University of British Columbia, Vancouver, BC, Canada

    Andrea Lee

  3. Department of Environmental Health and Safety, University of Minnesota Duluth, Duluth, MN, USA

    Jake Baxter

  4. Department of Physical Therapy, Marquette University, Marquette, MI, USA

    Sandra Hunter

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  1. Andrea Lee
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  2. Jake Baxter
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  3. Claire Eischer
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Correspondence to Tejin Yoon.

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Communicated by Nicolas Place.

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Lee, A., Baxter, J., Eischer, C. et al. Sex differences in neuromuscular function after repeated eccentric contractions of the knee extensor muscles. Eur J Appl Physiol 117, 1119–1130 (2017). https://doi.org/10.1007/s00421-017-3599-8

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  • DOI: https://doi.org/10.1007/s00421-017-3599-8

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