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Central activation, metabolites, and calcium handling during fatigue with repeated maximal isometric contractions in human muscle

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Abstract

Purpose

To determine the roles of calcium (Ca2+) handling by sarcoplasmic reticulum (SR) and central activation impairment (i.e., central fatigue) during fatigue with repeated maximal voluntary isometric contractions (MVC) in human muscles.

Methods

Contractile performance was assessed during 3 min of repeated MVCs (7-s contraction, 3-s rest, n = 17). In ten participants, in vitro SR Ca2+-handling, metabolites, and fibre-type composition were quantified in biopsy samples from quadriceps muscle, along with plasma venous [K+]. In 11 participants, central fatigue was compared using tetanic stimulation superimposed on MVC in quadriceps and adductor pollicis muscles.

Results

The decline of peak MVC force with fatigue was similar for both muscles. Fatigue resistance correlated directly with % type I fibre area in quadriceps (r = 0.77, P = 0.009). The maximal rate of ryanodine-induced Ca2+-release and Ca2+-uptake fell by 31 ± 26 and 28 ± 13%, respectively. The tetanic force depression was correlated with the combined reduction of ATP and PCr, and increase of lactate (r = 0.77, P = 0.009). Plasma venous [K+] increased from 4.0 ± 0.3 to 5.4 ± 0.8 mM over 1–3-min exercise. Central fatigue occurred during the early contractions in the quadriceps in 7 out of 17 participants (central activation ratio fell from 0.98 ± 0.05 to 0.86 ± 0.11 at 1 min), but dwindled at exercise cessation. Central fatigue was seldom apparent in adductor pollicis.

Conclusions

Fatigue with repeated MVC in human limb muscles mainly involves peripheral aspects which include impaired SR Ca2+-handling and we speculate that anaerobic metabolite changes are involved. A faster early force loss in quadriceps muscle with some participants is attributed to central fatigue.

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Abbreviations

ANOVA:

Analysis of variance

ATP:

Adenosine triphosphate

[Ca2+]:

Ca2+ concentration

CAR:

Central activation ratio

CF group:

Central fatigue group

CNS:

Central nervous system

Cr:

Creatine

[K+]v :

Plasma venous K+ concentration

MVC:

Maximum voluntary isometric contraction

[Na+]v :

Plasma venous Na+ concentration

NCF group:

Non-central fatigue group

PCr:

Phosphocreatine

Pi :

Inorganic phosphate

PRFD:

Peak rate of force development

PRR:

Peak rate of relaxation

r :

Pearson’s correlation coefficient

SD:

Standard deviation

SR:

Sarcoplasmic reticulum

%ΔSR:

% Change sarcoplasmic reticulum function

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Acknowledgements

We gratefully thank our enthusiastic participants, along with Dr. Xanne A.K. Janse de Jonge and Kylie Hoffman for help with experiments, and Dr. Grace Bryant for performing the muscle biopsies. There was no external funding for this project.

We salute our inspirational coauthor, friend, colleague, and mentor Martin W. Thompson who passed away during the course of this work.

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Authors and Affiliations

  1. Sports Performance Research Institute New Zealand, School of Sport and Recreation, Faculty of Health and Environmental Sciences, Auckland University of Technology, Private Bag 92006, Auckland, 1020, New Zealand

    Simeon P. Cairns

  2. Health and Rehabilitation Research Institute, Faculty of Health and Environmental Sciences, Auckland University of Technology, Auckland, New Zealand

    Simeon P. Cairns

  3. Exercise, Health and Performance Research Group, Faculty of Health Sciences, University of Sydney, Sydney, Australia

    Luke A. G. Inman, Patricia A. Ruell & Martin W. Thompson

  4. High Performance Sport New Zealand, Auckland, New Zealand

    Caroline P. MacManus

  5. Revant Rehabilitation Centres, Breda, The Netherlands

    Ingrid G. L. van de Port

  6. Department of Exercise Physiology, School of Medical Sciences, University of New South Wales, Sydney, Australia

    Jeanette M. Thom

Authors
  1. Simeon P. Cairns
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  2. Luke A. G. Inman
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  3. Caroline P. MacManus
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  4. Ingrid G. L. van de Port
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  5. Patricia A. Ruell
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  6. Jeanette M. Thom
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  7. Martin W. Thompson
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Correspondence to Simeon P. Cairns.

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Communicated by Nicolas Place.

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Cairns, S.P., Inman, L.A.G., MacManus, C.P. et al. Central activation, metabolites, and calcium handling during fatigue with repeated maximal isometric contractions in human muscle. Eur J Appl Physiol 117, 1557–1571 (2017). https://doi.org/10.1007/s00421-017-3640-y

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