Skeletal muscle fatigue during locomotion

Project overview

This project grant scheme was for early career researchers to gain funding to initiate a research programme. The specific project aimed to investigate various potential mechanisms of skeletal muscle fatigue that might explain the limits of locomotor performance observed in animals.

Project objectives

To build the equipment set-up required to use the work loop technique to undertake in vitro testing of muscle. To use the equipment to investigate the likely mechanisms of in vitro muscle fatigue during repeated cycles of length changes with active shortening.

• Impact statement

  This enabled us to build the equipment and validate the methodology for assessing isolated skeletal muscle fatigue under conditions that better simulated locomotor function. This underpinning project has since led to multiple projects and publications based on this methodology.

• Outputs

  Directly resulting from this project

  James, R.S., Wilson, R.S. and Askew G.N. (2004) The effects of caffeine on mouse skeletal muscle power output during recovery from fatigue. Journal of Applied Physiology 96, 545-552. DOI: 10.1152/japplphysiol.00696.2003

  Wilson, R.S. and James, R.S. (2004) Constraints on muscular performance: trade-offs between power output and fatigue resistance. Proceedings of the Royal Society B (Suppl.) 271, S222-S225. DOI: 10.1098/rsbl.2003.0143

  Wilson, R.S., James, R.S. and Van Damme, R.V. (2002) Trade-offs between speed and endurance in the frog Xenopus laevis: a multi-level approach. Journal of Experimental Biology 205, 1145-1152.

  Subsequent publications from projects based on this one

  1. Fletcher S., Maddock H., James R.S., Wallis R. and Gharanei M. (2020) The cardiac work-loop technique: An in vitro model for identifying and profiling drug-induced changes in inotropy using rat papillary muscles. Scientific Reports 10(1), 5258. doi: 10.1038/s41598-020-58935-2.
  2. Hill C., James R.S., Cox V.M., Seebacher, F. and Tallis J. (2020) Age-Related Changes in Isolated Mouse Skeletal Muscle Function are Dependent on Sex, Muscle & Contractility Mode. American Journal of Physiology 319(3), R296-R314. doi: 10.1152/ajpregu.00073.2020
  3. Padilla, P., Tallis J., Hurst J., Courant J., James R.S., Herrel A. (2020) Do muscle contractile properties drive differences in locomotor performance in invasive populations of Xenopus laevis, in France? Journal of Comparative Physiology B. 190 (6), 771–778. doi: 10.1007/s00360-020-01310-4
  4. Seebacher, F. and James, R.S. (2019) Increased physical activity does not improve obesity-induced decreases in muscle quality in zebrafish (Danio rerio). Journal of Applied Physiology 127(6), 1802-1808. doi: 10.1152/japplphysiol.00433.2019.
  5. Hill C., James R.S., Cox V.M. and Tallis J. (2019) Does dietary-induced obesity in old age impair the contractile performance of isolated mouse soleus, extensor digitorum longus and diaphragm skeletal muscles? Nutrients 2019, 11(3), 505. doi:10.3390/nu11030505
  6. Hurst J., James R.S., Cox V.M. and Tallis J. (2018) Investigating a dose response relationship between high fat diet consumption and the contractile performance of isolated mouse soleus, EDL and diaphragm muscles. European Journal of Applied Physiology 119(1), 213-226. doi:10.1007/s00421-018-4017-6
  7. Tallis J., Higgins M.F., Cox V.M., Duncan M.J., James R.S. (2018) An exercise induced improvement in isolated skeletal muscle contractility does not affect the ergogenic benefit of 70uM caffeine treatment. Journal of Experimental Biology 221, jeb190132. doi:10.1242/jeb.190132
  8. Hill C., James R.S., Cox V.M., Tallis J. (2018) The effect of increasing age on the concentric and eccentric contractile properties of isolated mouse soleus and extensor digitorum longus muscle. The Journals of Gerontology Series A 73(5), 579-587. DOI: 10.1093/gerona/glx243
  9. Tallis J., Higgins M.F., Seebacher F., Cox V.M., Duncan M.J., James R.S. (2017) The Effects of 8 Weeks of Voluntary Wheel Running on the Mechanical Performance of Isolated Locomotory (Soleus) and Respiratory (Diaphragm) Skeletal Muscle During Early Ageing. Journal of Experimental Biology 220, 3733-3741. doi: 10.1242/jeb.166603
  10. Seebacher F., Tallis J., Hill C., McShea K., James R.S. (2017) Obesity-induced decreases in muscle performance are not reversible by weight loss. International Journal of Obesity 41(8), 1271-1278. doi: 10.1038/ijo.2017.81
  11. Tallis J., Hill C., James R.S., Cox V.M., Seebacher F. (2017) The effect of obesity on the contractile performance of isolated mouse soleus, EDL and diaphragm muscle. Journal of Applied Physiology 122(1), 170-181. doi: 10.1152/japplphysiol.00836.2016
  12. Tallis, J., James R.S., Cox, V.M., Duncan, M. (2017) Is the Ergogenicity of Caffeine Affected by Increasing Age? The Direct Effect of a Physiological Concentration of Caffeine on the Power Output of Maximally Stimulated EDL and Diaphragm Muscle Isolated From the Mouse. Journal of Nutrition, Health and Aging 21(4), 440-448. doi:10.1007/s12603-016-0832-9
  13. James, R.S., Little, A.G., Tallis, J., and Seebacher, F. (2016) Thyroid hormone influences muscle mechanics in carp (Cyprinus carpio) independently from SERCA activity. Journal of Experimental Biology 219, 2806-2808. doi: 10.1242/jeb.143529
  14. Seebacher F., Webster M.M., James R.S., Tallis J., Ward A.J.W. (2016) Morphological differences between habitats are associated with physiological and behavioural trade-offs in stickleback (Gasterosteus aculeatus). Royal Society Open Science 3, doi: 10.1098/rsos.160316
  15. Seebacher, F., Little, A.G., James, R.S. (2015) Skeletal muscle contractile function predicts activity and behaviour in zebrafish. Journal of Experimental Biology 218, 3878-3884. doi:10.1242/jeb.129049
  16. James R.S., Vanhooydonck B., Tallis J.A., Herrel A. (2015) Larger lacertid lizard species produce higher iliotibialis muscle stress; the evolution of muscle contractile mechanics with body size in lacertid lizards. Journal of Experimental Biology 218, 3589-3595. doi: 10.1242/jeb.124974
  17. James R.S., Tallis J., Angilletta M. (2015) Regional thermal specialisation in a mammal: temperature affects power output of core muscle more than that of peripheral muscle in adult mice (Mus musculus). Journal of Comparative Physiology B. 185(1), 135-142. doi: 10.1007/s00360-014-0872-6
  18. Tallis J, James R.S., Little A.G., Cox V.M., Duncan M., Seebacher F. (2014) The Early Effects of Ageing on the Mechanical Performance of Isolated Locomotory (EDL) and Respiratory (diaphragm) Skeletal Muscle Using the Work Loop Technique. American Journal of Physiology R 307(6), R670-684. doi: 10.1152/ajpregu.00115.2014
  19. Seebacher F., Tallis J.A., James R.S. (2014) The cost of muscle power production: muscle oxygen consumption per unit work increases at low temperatures in Xenopus laevis Journal of Experimental Biology 217(11), 1940-1945. doi: 10.1242/​jeb.101147
  20. Vanhooydonck B., James R.S., Tallis J., Aerts P., Tadic Z., Tolley K. A., Measey J., Herrel A. (2014) Is the whole more than the sum of its parts? Evolutionary trade-offs between burst and sustained locomotion in lacertid lizards. Proceedings of the Royal Society B 281, 20132677. http://dx.doi.org/10.1098/rspb.2013.2677 
  21. Gharanei M., Hussain A., James R.S., Janneh O., Maddock H. (2014) Investigation into the cardiotoxic effects of doxorubicin on contractile function and the protection afforded by cyclosporin A using the work-loop assay. Toxicology In Vitro 28(5), 722-731. doi: 10.1016/j.tiv.2014.01.011
  22. Tallis, J., Higgins M., Cox, V.M., Duncan, M., James R.S. (2014) Does a Physiological Concentration of Taurine Increase Acute Muscle Power Output, Time to Fatigue, and Recovery in Isolated Mouse Soleus (Slow) Muscle With or Without the Presence of Caffeine? Canadian Journal of Physiology and Pharmacology 91, 42-49. dx.doi.org/10.1139/cjpp-2013-0195.
  23. James R.S., Staples J., Brown J.C.L., Tessier S. and Storey, K.B. (2013) The effects of hibernation on the contractile and biochemical properties of skeletal muscles in the thirteen-lined ground squirrel, Ictidomys tridecemlineatus. Journal of Experimental Biology 216, 2587-2594. DOI: 10.1242/jeb.080663
  24. Higgins, M.F., Tallis, J., Price, M.J and James, R.S. (2013) The effects of elevated levels of sodium bicarbonate (NaHCO₃) on the acute power output and time to fatigue of maximally stimulated mouse soleus and EDL muscles. European Journal of Applied Physiology 113(5), 1331-1341. DOI: 10.1007/s00421-012-2557-8
  25. Tallis, J., James R.S., Cox, V.M., Duncan, M (2013) Effect of caffeine on prolonged mammalian muscle performance at different activity levels. Journal of Physiological Sciences 63(2), 125-132. DOI 10.1007/s12576-012-0247-2
  26. Seebacher F., Pollard S.R. and James R.S. (2012) How well do muscle biomechanics predict whole-animal locomotor performance?: The role of Ca²⁺ handling. Journal of Experimental Biology 215, 1847-1853. DOI:10.1242/jeb.067918
  27. James R.S., Tallis, J., Herrel, A. and Bonneaud, C. (2012) Warmer is better: Thermal sensitivity of both maximal and sustained power output in the iliotibialis muscle isolated from adult Xenopus tropicalis. Journal of Experimental Biology 215, 552-558. DOI: 10.1242/​jeb.063396
  28. Tallis, J., James R.S., Cox, V.M., Duncan, M. (2012) The Effect of Physiological Concentrations of Caffeine on the Power Output of Maximally and Sub Maximally Stimulated Mouse EDL (Fast) and Soleus (Slow) Muscle. Journal of Applied Physiology 112, 64-71. DOI: 10.1152/japplphysiol.00801.2011
  29. James, R.S., Walter, I. and Seebacher, F. (2011) Variation in expression of calcium handling proteins is associated with inter-individual differences in mechanical performance of rat (Rattus norvegicus) skeletal muscle. Journal of Experimental Biology 214, 3542-3548. DOI: 10.1242/​jeb.058305
  30. James R.S., Tallis, J., Seebacher, F. and Storey, K. (2011) Daily torpor reduces mass and changes stress and power output of soleus and EDL muscles in the Djungarian hamster, Phodopus sungorus. Journal of Experimental Biology 214, 2896-2902. DOI: 10.1242/​jeb.057877
  31. Wilson, R.S., James, R.S., Bywater, C. and Seebacher, F. (2009) Costs and benefits of increased weapon size differ between sexes of the slender crayfish, Cherax dispar. Journal of Experimental Biology 212, 853-858. DOI: 10.1242/jeb.024547.
  32. Vassilakos, G., James, R.S. and Cox, V.M. (2009) Effect of stimulation frequency on force, net power output, and fatigue in mouse soleus muscle in vitro. Canadian Journal of Physiology and Pharmacology 87, 203-210. DOI: 10.1139/Y09-002.
  33. Seebacher, F. and James, R.S. (2008) Plasticity of muscle function in a thermoregulating ectotherm (Crocodylus porosus): biomechanics and metabolism. American Journal of Physiology 294, R1024-R1032. DOI: 10.1152/ajpregu.00755.2007.
  34. James, R.S. and Wilson, R.S. (2008) Explosive jumping: extreme morphological and physiological specialisations of Australian Rocket frogs (Litoria nasuta). Physiological and Biochemical Zoology 81, 176-185. DOI: 10.1086/525290.
  35. Drake, A. and James, R.S. (2008) Prediction of race walking performance via laboratory and field tests. New Studies in Athletics 23, 35-41.
  36. Wilson, R.S., Angilletta Jr., M.J., James, R.S., Navas, C.A. and Seebacher, F. (2007) Dishonest signals of strength in male slender crayfish (Cherax dispar) during agonistic encounters. American Naturalist 170, 284-291. DOI: 10.1086/519399.
  37. Herrel, A., James, R.S. and Van Damme, R. (2007) Fight versus flight: physiological basis for temperature dependent behavioral shifts in lizards. Journal of Experimental Biology 210, 1762-1767. DOI: 10.1242/jeb.003426.
  38. Van Wassenbergh, S., Herrel, A., James, R.S. and Aerts, P. (2007) Scaling of contractile properties of catfish feeding muscles. Journal of Experimental Biology 210, 1183-1193. DOI: 10.1242/jeb.000109.
  39. James, R.S., Navas, C.A. and Herrel, A. (2007) How important are skeletal muscle mechanics in setting limits on jumping performance? Journal of Experimental Biology 210, 923-933. Review paper. DOI: 10.1242/jeb.02731
  40. Symonds, B.L., James, R.S. and Franklin, C.E. (2007) Getting the jump on skeletal muscle disuse atrophy: preservation of contractile performance in aestivating Cyclorana alboguttata (Günther, 1867). Journal of Experimental Biology 210, 825-835. DOI: 10.1242/jeb.02711
  41. Navas, C.A. and James, R.S. (2007) Sexual dimorphism of extensor carpi radialis muscle size, isometric force, relaxation rate and stamina during the breeding season of the frog Rana temporaria Linnaeus 1758. Journal of Experimental Biology 210, 715-721. DOI: 10.1242/jeb.000646.
  42. James, R.S., Wilson, R.S., Carvalho, J.E., Kohlsdorf, T., Gomes, F.R. and Navas, C.A. (2005) Inter-individual differences in leg muscle mass and pyruvate kinase activity correlate with inter-individual differences in jumping performance of Hyla multilineata. Physiological and Biochemical Zoology 78(5), 857-867. DOI: 10.1086/432149
  43. James, R.S., Kohlsdorf, T., Cox, V.M. and Navas, C.A. (2005) 70mM caffeine treatment enhances in vitro force and power output during cyclic activities in mouse extensor digitorum longus muscle. European Journal of Applied Physiology 95, 74-82. DOI: 10.1016/j.cattod.2005.04.009
  44. James, R.S., Wilson, R.S. and Askew G.N. (2004) The effects of caffeine on mouse skeletal muscle power output during recovery from fatigue. Journal of Applied Physiology 96, 545-552. DOI: 10.1152/japplphysiol.00696.2003
  45. Wilson, R.S. and James, R.S. (2004) Constraints on muscular performance: trade-offs between power output and fatigue resistance. Proceedings of the Royal Society B (Suppl.) 271, S222- DOI: 10.1098/rsbl.2003.0143
  46. Wilson, R.S., James, R.S., Kohlsdorf, T. and Cox, V.M. (2004) Inter-individual variation of isolated muscle performance and structure in the toad Bufo viridis. Journal of Comparative Physiology B. 174, 453-459. DOI: 10.1007/s00360-004-0431-7
  47. Navas, C.A., Jared, C., Carvalho, J.E., Chaui-Berlink, J.G., Pai Silva, M.D., Antoniazzi, M., James, R.S., Wilson, R.S., and Kohlsdorf, T. (2004) Morphological and physiological specialization for digging in the amphisbaenians an ancient lineage of fossorial vertebrates. Journal of Experimental Biology 207, 2433-2441. DOI: 10.1242/jeb.01041
  48. Kohlsdorf, T., James, R.S., Carvalho, J.E., Wilson, R.S., Pae-Silva M.D. and Navas C.A. (2004) Locomotor performance of closely related Tropidurus species: relationships with physiological parameters and ecological divergence. Journal of Experimental Biology 207, 1183-1192. DOI: 10.1242/jeb.00870