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Sex differences in muscle fatigability and activation patterns of the human quadriceps femoris

Abstract

The purposes of this study were to determine if the fatigability of the quadriceps femoris varies by biological sex under conditions of normal muscle blood flow and ischemia, and if differences in neuromuscular activation patterns exist. Young men and women (n=11/group; age 20–39 years) performed a sustained knee extension contraction at 25% of maximal force under conditions of occluded (OCC) and normal muscle blood flow (NON-OCC). Electromyographic (EMG) activity was recorded from the vastus lateralis (VL), rectus femoris (RF), vastus medialis (VM) and biceps femoris (BF) muscles, and analyzed for fatigue-induced changes in the amplitude and burst rate and duration (transient changes in motor unit recruitment) of the signal. Additionally, force fluctuations during the sustained contraction were quantified. Women had a longer time to task failure during the NON-OCC task [214.9±20.5 vs. 169.1±20.5 (SE) s] (P=0.02), but not during the OCC task (179.6+19.6 vs. 165.2±19.6 s). EMG data demonstrated sex differences in the neuromuscular activation pattern of the RF muscle and the collectively averaged QF muscles. During the NON-OCC and OCC tasks women achieved a higher relative activation of the RF at task failure than men (NON-OCC: 40.68±4.57 vs. 24.49±4.19%; OCC: 36.80±5.45 vs. 24.41±2.12%) (P=0.02 and 0.05, respectively). Also, during both tasks, they demonstrated a greater relative activation at task failure than men when an average of the VL, VM and RF was considered. Additionally, women exhibited a greater coefficient of variation in force fluctuations during the last-third of the fatiguing NON-OCC task (6.21±0.567 vs. 4.56±0.56%) (P=0.001). No sex differences in EMG burst rate or duration were observed, although there was a trend towards greater EMG burst rate of the RF in association with muscle fatigue in the women (P=0.09). Interestingly, the only neuromuscular activation variable that displayed a significant relationship with the time to task failure was the average relative EMG of the QF at task failure, and this relationship was observed under both experimental blood flow conditions (NON-OCC: r=0.47, P=0.03; OCC: r=0.44, P=0.04). These results indicate that sex differences in muscle blood flow and/or muscle metabolism are in part responsible for the female advantage in fatigue-resistance. Additionally, these findings suggest that men synergistically recruit the RF compartment to a lesser extent than women in association with muscle fatigue, and that women achieve an overall greater relative activation of the QF at task failure than men. However, the implications of these sex differences in neuromuscular activation patterns during fatiguing muscular contractions on the ability to withstand muscle fatigue (prolonged time to task failure) does not appear to be causally related.

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References

  1. Ainsworth BE, Jacobs DR, Leon AS (1993) Validity and reliability of self-reported phsyical activity status: the Lipid Research Clinics questionnaire. Med Sci Sports Exerc 25:92–98

    Google Scholar 

  2. Basmaijian JV, DeLuca CL (1985) Muscle alive—their functions revealed by electromyography. Williams and Wilkins, Baltimore

    Google Scholar 

  3. Bonde-Petersen F, Robertson CH Jr (1981) Blood flow in “red” and “white” calf muscles in cats during isometric and isotonic exercise. Acta Physiol Scand 112:243–251

    Google Scholar 

  4. Clark BC, Manini TM, Thé DJ, Doldo NA, Ploutz-Snyder LL (2003) Gender differences in skeletal muscle fatigability are related to contraction type and EMG spectral compression. J Appl Physiol 94:2263–2272

    Google Scholar 

  5. Clark BC, Collier SR, Manini TM, Ploutz-Snyder LL (2004) Sex differences in muscle fatigability and activation patterns of the human quadriceps femoris. Med Sci Sports Exerc 36(5):S277

    Article  Google Scholar 

  6. Cram JR, Kasman GS (1998) Introduction to surface electromyography. Aspen, Gaithersburg

    Google Scholar 

  7. Enoka RM, Stuart DG (1992) Neurobiology of muscle fatigue. J Appl Physiol 72:1631–1648

    Google Scholar 

  8. Fuglevand AJ, Zackowski KM, Huey KA, Enoka RM (1993) Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol 460:549–572

    Google Scholar 

  9. Fulco CS, Cymerman A, Muza SR, Rock PB, Pandolf KB, Lewis SF (1994) Adductor pollicis muscle fatigue during acute and chronic altitude exposure and return to sea level. J Appl Physiol 77:179–183

    Google Scholar 

  10. Fulco CS, Rock PB, Muza SR, Lammi E, Cymerman A, Butterfield G, Moore LG, Braun B, Lewis SF (1999) Slower fatigue and faster recovery of the adductor pollicis muscle in women matched for strength with men. Acta Physiol Scand 167:233–239

    Article  Google Scholar 

  11. Hakkinen K (1993) Neuromuscular fatigue and recovery in male and female athletes during heavy resistance exercise. Int J Sports Med 14:53–59

    Google Scholar 

  12. Hatzikotoulas K, Siatras T, Spyropoulou E, Paraschos I, Patikas D (2004) Muscle fatigue and electromyographic changes are not different in women and men matched for strength. Eur J Appl Physiol 92:298–304

    Article  Google Scholar 

  13. Hicks AL, Kent-Braun JA, Ditor DS (2001) Sex differences in human skeletal muscle fatigue. Exerc Sport Sci Rev 29:109–112

    Article  Google Scholar 

  14. Hogan MC, Richardson RS, Kurdak SS (1994) Initial fall in skeletal muscle force development during ischemia is related to oxygen availability. J Appl Physiol 77:2380–2384

    Google Scholar 

  15. Hogan MC, Kohin S, Stary CM, Hepple RT (1999) Rapid force recovery in contracting skeletal muscle after brief ischemia is dependent on oxygen avaliability. J Appl Physiol 87:2225–2229

    Google Scholar 

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

    Google Scholar 

  17. Hunter SK, Enoka RM (2003) Changes in muscle activation can prolong the endurance time of a submaximal isometric contraction in humans. J Appl Physiol 94:108–118

    Google Scholar 

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

    Article  Google Scholar 

  19. Kagaya A, Homma S (1997) Brachial arterial blood flow during static handgrip exercise of short duration at varying intensities studied by a Doppler ultrasound method. Acta Physiol Scand 160:257–265

    Article  Google Scholar 

  20. Kent-Braun JA, Ng AV, Doyle JW, Towse TF (2002) Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J Appl Physiol 93:1813–1823

    Google Scholar 

  21. Kouzaki M, Shinohara M, Masani K, Kanehisa H, Fukunaga T (2002) Alternate muscle activity observed between knee extensor synergists during low-level sustained contractions. J Appl Physiol 93:675–684

    Google Scholar 

  22. Kouzaki M, Shinohara M, Mmasani K, Tachi M, Kanehisa H, Fukunaga T (2003) Local blood circulation among knee extensor synergists in relation to alternate muscle activity during low-level sustained contraction. J Appl Physiol 95:49–56

    Google Scholar 

  23. Laidlaw DH, Bilodeau M, Enoka RM (2000) Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve 23:600–612

    Google Scholar 

  24. Lanza IR, Towse TF, Caldwell GE, Wigmore DM, Kent-Braun JA (2003) Effects of age on human muscle torque, velocity, and power in two muscle groups. J Appl Physiol 95:2361–2369

    Google Scholar 

  25. Löscher WN, Cresswell AG, Thortensson A (1996) Excitatory drive to the alpha-motoneuron pool during a fatiguing submaximal contraction in man. J Physiol 491:271–280

    Google Scholar 

  26. McComas AJ (1996) Skeletal muscle: form and function. Human Kinetics, Champaign, Ill.

    Google Scholar 

  27. Miller AE, MacDougall JD, Tarnopolsky MA, Sale DG (1993) Gender differences in strength and muscle fiber characteristics. Eur J Appl Physiol Occup Physiol 66:254–262

    Article  Google Scholar 

  28. Mosso A (1904) Fatigue. Swan Sonnenschein, London

    Google Scholar 

  29. Robertson RJ, Gross FL, Rutkowski J, Lenz B, Dixon C, Timmer J, Frazee K, Dube J, Andreacci J (2003) Concurrent validation of the OMNI perceived exertion scale for resistance exercise. Med Sci Sports Exerc 35:333–341

    Google Scholar 

  30. Rochette L, Hunter SK, Place N, Lepers R (2003) Activation varies among the knee extensor muscles during a submaximal fatiguing contraction in the seated and supine postures. J Appl Physiol 95:1515–1522

    Google Scholar 

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

    Google Scholar 

  32. 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

    CAS  PubMed  Google Scholar 

  33. Semmler JG (2002) Motor unit synchronization and neuromuscular performance. Exerc Sport Sci Rev 30:8–14

    Article  PubMed  Google Scholar 

  34. Semmler JG, Kutzscher DV, Enoka RM (1999) Gender differences in the fatigability of human skeletal muscle. J Neurophysiol 82:3590–3593

    Google Scholar 

  35. Shinohara M, Yoshitake Y, Kouzaki M, Fukuoka H, Fukunaga T (2003) Strength training counteracts motor performance losses during bed rest. J Appl Physiol 95:1485–1492

    Google Scholar 

  36. Sjogaard G, Savard G, Juel C (1988) Muscle blood flow during isometric activity and its relation to muscle fatigue. Eur J Appl Physiol 57:327–335

    Article  Google Scholar 

  37. 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 48:623–629

    Google Scholar 

  38. Tamaki H, Kitada K, Akamine T, Murata F, Sakou T, Kurata H (1998) Alternate activity in the synergistic muscles during prolonged low-level contractions. J Appl Physiol 84:1943–1951

    Google Scholar 

  39. West W, Hicks A, Clements L, Dowling J (1995) The relationship between voluntary electromyogram, endurance time and intensity of effort in isometric handgrip exercise. Eur J Appl Physiol Occup Physiol 71:301–305

    Article  Google Scholar 

  40. Westgaard RH, De Luca CJ (1999) Motor unit substitution in long-duration contractions of the human trapezius muscle. J Neurophysiol 82:501–504

    CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported in part by awards from the Mid-Atlantic Regional Chapter of the American College of Sports Medicine and Syracuse University. This experiment complied with the current laws of the country in which it was performed (United States of America).

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Correspondence to Brian C. Clark.

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Clark, B.C., Collier, S.R., Manini, T.M. et al. Sex differences in muscle fatigability and activation patterns of the human quadriceps femoris. Eur J Appl Physiol 94, 196–206 (2005). https://doi.org/10.1007/s00421-004-1293-0

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Keywords

  • Gender
  • Muscle fatigue
  • Bursting
  • Knee extensors
  • Ischemia