Skip to main content
Log in

Strategies that improve human skeletal muscle performance during repetitive, non-isometric contractions

  • Neuromuscular Function
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

Previous studies have suggested that during sustained maximal voluntary and evoked contractions, decreasing activation rates may minimize fatigue. The idea of gradually decreasing stimulation frequency to preserve force during fatiguing isometric contractions has, however, recently been challenged. The primary purpose of this study was to test the effectiveness of decreasing or increasing electrical stimulation rates during evoked, repetitive, submaximal, non-isometric contractions of healthy human quadriceps femoris muscles. The ability of the muscles to produce a 50° knee excursion repetitively was evaluated using low-frequency trains, high-frequency trains, and a combination of these trains. Results showed that stimulating the muscles with high-frequency trains followed by low-frequency trains produced the worst performance and starting with low-frequency trains followed by high-frequency trains produced the best performance. Present results cast doubt on the applicability of decreasing stimulation rates during non-isometric contractions and suggest that a combination of trains that begin at a low frequency and then switch to a higher-frequency may improve performance during functional electrical stimulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3. A
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Adam A, De Luca CJ (2003) Recruitment order of motor units in human vastus lateralis muscle is maintained during fatiguing contractions. J Neurophysiol 90:2919–2927

    PubMed  Google Scholar 

  2. Barnett S, Cooney K, Johnston R (1991) Electrically elicited quadriceps femoris muscle torque as a function of various electrode placements. J Clin Electrophysiol 3:5–8

    Google Scholar 

  3. Bevan L, Laouris Y, Reinking RM, Stuart DG (1992) The effect of the stimulation pattern on the fatigue of single motor units in cats. J Physiol (Lond) 449:85–108

    Google Scholar 

  4. Bigland-Ritchie BR (1993) Regulation of motorneuron firing rates in fatigue. In: Sargeant AJ, Kernell D (eds) Neuromuscular fatigue. Royal Netherlands Academy of Arts and Sciences, Amsterdam, pp147–155

  5. Bigland-Ritchie B, Jones DA, Woods JJ (1979) Excitation frequency and muscle fatigue: electrical responses during human voluntary and stimulated contractions. Exp Neurol 64:414–427

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  7. Bigland-Ritchie B, Johansson R, Lippold OCJ, Smith S, Woods JJ (1983) Changes in motorneuron firing rates during sustained maximal voluntary contractions. J Physiol (Lond) 340:335–346

    Google Scholar 

  8. Bigland-Ritchie B, Cafarelli E, Vollestad NK (1986) Fatigue of submaximal static contractions. Acta Physiol Scand 128:137–148

    Google Scholar 

  9. Binder-Macleod SA, Barrish WJ (1992) Force response of rat soleus muscle to variable-frequency train stimulation. J Neurophysiol 68:1068–1078

    CAS  PubMed  Google Scholar 

  10. Binder-Macleod SA, Lee SCK (1996) Catchlike property of human skeletal muscle during isovelocity movements. J Appl Physiol 80:2051–2059

    Google Scholar 

  11. Binder-Macleod SA, McDermond LR (1992) Changes in the force-frequency relationship of the human quadriceps muscle following electrically and voluntarily induced fatigue. Phys Ther 72:95–104

    CAS  PubMed  Google Scholar 

  12. Binder-Macleod SA, Scott WB (2001) Comparison of fatigue produced by various electrical stimulation trains. Acta Physiol Scand 172:195–203

    Article  CAS  PubMed  Google Scholar 

  13. Binder-Macleod SA, Halden EE, Jungles KA (1995) Effects of stimulation intensity on the physiological responses of human motor units. Med Sci Sports Exerc 27:556–565

    CAS  PubMed  Google Scholar 

  14. Binder-Macleod SA, Lee SCK, Fritz AD, Kucharski LJ (1998) New look at force-frequency relationship of human skeletal muscle: effects of fatigue. J Neurophysiol 79:1858–1868

    CAS  PubMed  Google Scholar 

  15. Burke RE (1981) Motor units: anatomy, physiology and functional organization. In: Brooks VB (ed) Handbook of physiology, vol 2. Williams and Wilkins, Baltimore, MD, pp 345–411

  16. Burke RE, Rudomin P, Zajac FE III (1976) The effect of activation history on tension production by individual muscle units. Brain Res 109:515–529

    CAS  PubMed  Google Scholar 

  17. Chin ER, Allen DG (1996) The role of elevations in intracellular [Ca2+] in the development of low frequency fatigue in mouse single fibers. J Physiol (Lond) 491:813–824

    Google Scholar 

  18. Damiano DL, Martellotta TL, Sullivan DJ, Granata KP (2000) Muscle force production and functional performance in spastic cerebral palsy: relationship of cocontraction. Arch Phys Med Rehabil 81:895–900

    Google Scholar 

  19. Ding J, Wexler AS, Binder-Macleod SA (2000) Development of a mathematical model that predicts optimal muscle activation pattern. J Appl Physiol 88:916–925

    Google Scholar 

  20. Duchateau J, Hainaut K (1986) Nonlinear summation of contractions in striated muscle. II. Potentiation of intracellular Ca2+ movements in single barnacle muscle fibers. J Muscle Res Cell Motil 7:12–24

    Google Scholar 

  21. Edwards RHT, Hill DK, Jones DA, Merton PA (1977) Fatigue of long duration in human skeletal muscle after exercise. J Physiol (Lond) 272:769–778

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  23. Korzeniewski B, Zoladz JA (2003) Training-induced adaptation of oxidative phosphorylation in skeletal muscles. Biochem J 374:37–40

    Article  CAS  PubMed  Google Scholar 

  24. Fitts RH (1994) Cellular mechanisms of muscle fatigue. Physiol Rev 74:49–94

    CAS  PubMed  Google Scholar 

  25. Fuglevand AJ (1996) Neural aspects of fatigue. Neuroscientist 2:203–206

    Google Scholar 

  26. Fuglevand AJ, Keen DA (2003) Re-evaluation of muscle wisdom in human adductor pollicis using physiological rates of stimulation. J Physiol (Lond) 549:865–875

    Google Scholar 

  27. Fuglevand AJ, Macefield VG, Bigland-Ritchie B (1999) Force-frequency and fatigue properties of motor units in muscles that control digits of the human hand. J Neurophysiol 81:1718–1729

    CAS  PubMed  Google Scholar 

  28. Garland SJ, Gossen ER (2002) The muscle wisdom hypothesis in human muscle fatigue. Exerc Sport Sci Rev 30:45–49

    Article  PubMed  Google Scholar 

  29. Garland SJ, Enoka RM, Serrano LP, Robinson GA (1994) Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. J Appl Physiol 76:2411–2419

    CAS  PubMed  Google Scholar 

  30. Garland SJ, Griffin L, Ivanova T (1997) Motor unit discharge rate is not associated with muscle relaxation in sustained submaximal contractions in humans. Neurosci Lett 239:25–28

    CAS  PubMed  Google Scholar 

  31. Griffin L, Garland SJ, Ivanova T, Gossen ER (2001) Muscle vibration sustains motor unit firing rate during submaximal isometric fatigue in humans. J Physiol (Lond) 535:929–936

    Google Scholar 

  32. Henneman E, Mendell LM (1981) Functional organization of motor neuron pool and its inputs. In: Brooks VB (ed) Handbook of Physiology, vol 2. Williams and Wilkins, Baltimore, MD, pp 423–508

  33. Jones DA, Bigland-Ritchie B, Edwards RHT (1979) Excitation frequency and muscle fatigue: Mechanical responses during voluntary and stimulated contractions. Exp Neurol 64:401–413

    CAS  PubMed  Google Scholar 

  34. Karu ZZ, Durfee WK, Barzilai AM (1995) Reducing muscle fatigue in FES applications by stimulating with N-let pulse trains. IEEE Trans Biomed Eng 42:809–817

    Article  CAS  PubMed  Google Scholar 

  35. Kebaetse MB, Lee SCK, Binder-Macleod SA (2001) A novel stimulation pattern improves performance during repetitive dynamic contractions. Muscle Nerve 24:744–752

    Article  CAS  PubMed  Google Scholar 

  36. Kebaetse MB, Turner AE, Binder-Macleod SA (2002) Stimulation pattern and frequency affect dynamic shortening contractions. J Appl Physiol 92:109–116

    PubMed  Google Scholar 

  37. Keppel G (1991) Correction for cumulative type I error. In: Keppel G (ed) Design and analysis: a researcher’s handbook, 3rd edn. Prentice Hall, Upper Saddle River, NJ, pp 163–184

  38. Knaflitz M, Merletti, De Luca CJ (1990) Inference of motor unit recruitment order in voluntary and electrically elicited contractions. J Appl Physiol 68:1657–1667

    PubMed  Google Scholar 

  39. Kukulka CG, Clamann HP (1981) Comparison of the recruitment and discharge properties of motor units in human brachial biceps and adductor pollicis during isometric contractions. Brain Res 219:45–55

    CAS  PubMed  Google Scholar 

  40. Lee SCK, Binder-Macleod SA (2000) Effects of activation frequency on dynamic performance of human fresh and fatigued muscles. J Appl Physiol 88:2166–2175

    Google Scholar 

  41. Lee SCK, Becker CN, Binder-Macleod SA (1999) Catchlike-inducing train activation of human muscle during isotonic contractions: burst modulation. J Appl Physiol 87:1758–1767

    CAS  PubMed  Google Scholar 

  42. Lewek M, Rudolph K, Axe M, Snyder-Mackler L (2002) The effect of insufficient quadriceps strength on gait after anterior cruciate ligament reconstruction. Clin Biomech 17:56–63

    Article  Google Scholar 

  43. Marsden CD, Meadows JC, Merton PA (1976) Fatigue of human muscle in relation to the number and frequency of motor impulses (abstract). J Physiol (Lond) 258:94–95

    Google Scholar 

  44. Marsden CD, Meadows JC, Merton PA (1983) “Muscular wisdom” that minimizes fatigue during prolonged effort in man: peak rates of motorneuron discharge and slowing of discharge during fatigue. Adv Neurol 39:351–366

    Google Scholar 

  45. Maton B, Gamet D (1989) The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: an EMG study. Eur J Appl Physiol 58:369–374

    CAS  Google Scholar 

  46. Miller KJ, Garland SJ, Ohtsuki T (1996) Motor unit behavior in humans during fatiguing arm movements. J Neurophysiol 75:1629–1636

    CAS  PubMed  Google Scholar 

  47. Russ DW, Binder-Macleod SA (1999) Variable-frequency trains offset low-frequency fatigue in human skeletal muscle. Muscle Nerve 22:874–882

    Article  CAS  PubMed  Google Scholar 

  48. Russ DW, Elliott MA, Vandenborne K, Walter GA, Binder-Macleod SA (2002) Metabolic costs of isometric force generation and maintenance of human skeletal muscle. Am J Physiol 282: E448–E457

    CAS  Google Scholar 

  49. Sandercock TG, Heckman CJ (1997) Doublet potentiation during eccentric and concentric contractions of cat soleus muscle. J Appl Physiol 82:1219–1228

    Google Scholar 

  50. Scott WB, Binder-Macleod SA (2003) Changing stimulation pattern improves performance during electrically elicited contractions. Muscle Nerve 28:174–180

    Article  PubMed  Google Scholar 

  51. Steele DS, Duke AM (2003) Metabolic factors contributing to altered Ca2+ regulation in skeletal muscle fatigue. Acta Physiol Scand 179:39–48

    Article  CAS  PubMed  Google Scholar 

  52. Stein RB, Parmiggiani F (1979) Optimal motor patterns for activating mammalian muscle. Brain Res 175:372–376

    Article  CAS  PubMed  Google Scholar 

  53. Stokes MJ, Edwards RHT, Cooper RG (1989) Effect of low frequency fatigue on human muscle strength and fatigability during subsequent stimulated activity. Eur J Appl Physiol 59:278–283

    Google Scholar 

  54. Thomas CK, Bigland-Ritchie B, Johansson R (1991) Force-frequency relationship of human thenar motor units. J Neurophysiol 65:1509–1516

    CAS  PubMed  Google Scholar 

  55. Westerblad H, Duty S, Allen DG (1993) Intracellular calcium concentration during low-frequency fatigue in isolated single fibers of mouse skeletal muscles. J Appl Physiol 75:382–388

    CAS  PubMed  Google Scholar 

  56. Williams JH (1997) Contractile apparatus and sarcoplasmic reticulum function: effects of fatigue, recovery, and elevated Ca2+. J Appl Physiol 83:444–450

    Google Scholar 

Download references

Acknowledgements

This research was supported by the National Institutes of Health grant HD 36797 to Dr. S.A. Binder-Macleod.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stuart A. Binder-Macleod.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kebaetse, M.B., Binder-Macleod, S.A. Strategies that improve human skeletal muscle performance during repetitive, non-isometric contractions. Pflugers Arch - Eur J Physiol 448, 525–532 (2004). https://doi.org/10.1007/s00424-004-1279-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-004-1279-0

Keywords

Navigation