Skip to main content
Log in

Abstract

This review focuses on the effects of temperature on the functioning of the neuromuscular system. The changes in environmental temperature could affect the contractile acts in both ectotherms and endotherms by changing the amplitude and velocity of contractions and, accordingly, the mechanical work of skeletal muscles. In this study, we summarize the data on the effects of hypo- and hyperthermia on the supraspinal and peripheral components of regulation of the neuromuscular function.

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.

Similar content being viewed by others

References

  1. Angilletta M.J. 2009. Thermal adaptation. A theoretical and empirical synthesis. Oxford: Oxford University Press.

    Book  Google Scholar 

  2. James R.S. 2013. A review of the thermal sensitivity of the mechanics of vertebrate skeletal muscle. J. Comp. Physiol. B. 183, 723–733.

    Article  PubMed  Google Scholar 

  3. Castellani J.W., Tipton M.J. 2015. Cold stress effects on exposure tolerance and exercise performance. Comp. Physiol. 6 (1), 443–469.

    Article  Google Scholar 

  4. Bennett A.F. 1990. Thermal dependence of locomotor capacity. Am. J. Physiol. 259, R253–R258.

    CAS  PubMed  Google Scholar 

  5. Racinais S., Oksa J. 2010. Temperature and neuromuscular function. Scand. J. Med. Sci. Sports. 20, 1–18.

    Article  PubMed  Google Scholar 

  6. Refinetti R. 1999. Amplitude of the daily rhythm of body temperature in eleven mammalian species. J. Therm. Biol. 24, 477–481.

    Article  Google Scholar 

  7. Wooden K.M., Walsberg G.E. 2004. Body temperature and locomotor capacity in a heterothermic rodent. J. Exp. Biol. 207, 41–46.

    Article  PubMed  Google Scholar 

  8. Ducharme M.B., Van Helder W.P., Radomski M.W. 1991. Tissue temperature profile in the human forearm during thermal stress at thermal stability. J. Appl. Physiol. 71, 1973–1978.

    CAS  PubMed  Google Scholar 

  9. Ranatunga K.W. 1998. Temperature dependence of mechanical power output in mammalian skeletal muscle. Exp. Physiol. 83, 371–376.

    Article  CAS  PubMed  Google Scholar 

  10. Bennett A.F. 1984. Thermal dependence of muscle function. Am. J. Physiol. 247, R217–R229.

    CAS  PubMed  Google Scholar 

  11. Rall J.A., Woledge R.C. 1990. Influence of temperature on mechanics and energetics of muscle contraction. Am. J. Physiol. 259, R197–R203.

    CAS  PubMed  Google Scholar 

  12. Marsh R.L. 1994. Jumping ability of anurans. In: Comparative vertebrate exercise physiology. Ed. Jones J.H. San Diego: Acad. Press, pp. 51–111.

    Google Scholar 

  13. Syme D.A. 2006. Functional properties of skeletal muscle. In: Fish physiology: Fish biomechanics. Ed. Randall D.J., Farrell A.P. Acad. Press, Elsevier, vol. 23, pp. 179–240.

    Google Scholar 

  14. Seebacher F., James R.S. 2008. Plasticity of muscle function in a thermoregulating ectotherm (Crocodylus porosus): Biomechanics and metabolism. Am. J. Physiol. 294, R1024–R1032.

    CAS  Google Scholar 

  15. Saltin B., Gagge A.P., Stolwijk J.A. 1968. Muscle temperature during submaximal exercise in man. J. Appl. Physiol. 25, 679–688.

    CAS  PubMed  Google Scholar 

  16. Kenny G.P., Reardon F.D., Zaleski W., Reardon M.L., Haman F., Ducharm M.B. 2003. Muscle temperature transients before, during, and after exercise measured using an intramuscular multisensor probe. J. Appl. Physiol. 94, 2350–2357.

    Article  CAS  PubMed  Google Scholar 

  17. Yaicharoen P., Wallman K., Morton A., Bishop D. 2012. The effect of warm-up on intermittent sprint performance and selected thermoregulatory parameters. J. Sci. Med. Sport. 15, 451–456.

    Article  PubMed  Google Scholar 

  18. Huxley A.F. 1964. Muscle. Annu. Rev. Physiol. 26, 131–152.

    Article  CAS  PubMed  Google Scholar 

  19. Rowlerson A.M., Spurway N.C. 1988. Histochemical and immunohistochemical properties of skeletal muscle fibres from Rana and Xenopus. Histochem. J. 20, 657–673.

    Article  Google Scholar 

  20. Grishin S.N., Ziganshin A.U. 2015. Synaptic organization of tonic motor units in vertebrates. Biochemistry (Moscow) Suppl. Series A: Membrane and Cell Biology. 9 (1), 13–20.

    Article  Google Scholar 

  21. Bulochnik E.D., Ziablov M.P. 1977. Effect of hyperthermia induced by a high ambient temperature on the direct cortical response. Bull. Eksp. Biol. Med. (Rus.). 84, 657–660.

    CAS  Google Scholar 

  22. Nybo L., Nielsen B. 2001. Middle cerebral artery blood velocity is reduced with hyperthermia during prolonged exercise in humans. J. Physiol. 534, 279–286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Nybo L., Secher N.H., Nielsen B. 2002. Inadequate heat release from the human brain during prolonged exercise with hyperthermia. J. Physiol. 545, 697–704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Rasmussen P., Stie H., Nybo L., Nielsen B. 2004. Heat induced fatigue and changes of the EEG is not related to reduced perfusion of the brain during prolonged exercise in humans. J. Thermal. Biol. 29, 731–737.

    Article  Google Scholar 

  25. Nunneley S.A., Martin C.C., Slauson J.W., Hearon C.M., Nickerson L.D.H., Mason P.A. 2002. Changes in regional cerebral metabolism during systemic hyperthermia in humans. J. Appl. Physiol. 92, 846–851.

    Article  PubMed  Google Scholar 

  26. Rasmussen P., Nybo L., Volianitis S., Moller K., Secher N.H., Gjedde A. 2010. Cerebral oxygenation is reduced during hyperthermic exercise in humans. Acta Physiol. 199, 63–70.

    Article  CAS  Google Scholar 

  27. Morrison S.A., Sleivert G.G., Neary J.P., Cheung S.S. 2009. Prefrontal cortex oxygenation is preserved and does not contribute to impaired neuromuscular activation during passive hyperthermia. Appl. Physiol. Nutr. Metab. 34, 66–74.

    Article  PubMed  Google Scholar 

  28. Nielsen B., Hyldig T., Bidstrup F., Gonzalez-Alonso J., Christoffersen G.R.J. 2001. Brain activity and fatigue during prolonged exercise in the heat. Pflügers Arch.–Eur. J. Physiol. 442, 41–48.

    Article  CAS  Google Scholar 

  29. Nybo L., Nielsen B. 2001. Perceived exertion is associated with an altered brain activity during exercise with progressive hyperthermia. J. Appl. Physiol. 91, 2017–2023.

    CAS  PubMed  Google Scholar 

  30. Racinais S., Gaoua N., Grantham J. 2008. Hyperthermia impairs short-term memory and peripheral motor drive transmission. J. Physiol. 586, 4751–4762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Davis S.L., Frohman T.C., Crandall C.G., Brown M.J., Mills D.A., Kramer P.D., Stüve O., Frohman E.M. 2008. Modeling Uhthoff’s phenomenon in MS patients with internuclear ophthalmoparesis. Neurology. 70, 1098–1106.

    Article  CAS  PubMed  Google Scholar 

  32. Katz B., Miledi R. 1965. Propagation of electric activity in motor nerve terminals. Proc. R. Soc. Lond. B. Biol. Sci. 161, 453–482.

    Article  CAS  PubMed  Google Scholar 

  33. Samigullin D., Bukharaeva E., Nikolsky E., Vyskocil F. 2003. Temperature effect on proximal to distal gradient of quantal release of acetylcholine at frog endplate. Neurochem. Res. 28 (3–4), 507–514.

    Article  CAS  PubMed  Google Scholar 

  34. Nicholls J.G., Martin A.R., Wallace B.G., Fuchs P.A. 2001. From neuron to brain. Sunderland, MA,USA: Sinauer Associates.

  35. Katz B. 2003. Neural transmitter release: From quantal secretion to exocytosis and beyond. J. Neurocytol. 32 (5-8), 437–446.

    Article  CAS  PubMed  Google Scholar 

  36. Vyskocil F., Illes P. 1977. Non-quantal release of transmitter at mouse neuromuscular junction and its dependence on the activity of Na+-K+ ATP-ase. Pflügers Arch. 370, 295–297.

    Article  CAS  PubMed  Google Scholar 

  37. Malomouzh A.I., Nikolsky E.E. 2010. Non-quantal release of transmitter: A myth or reality? Usp. Fiziol. Nauk (Rus.). 41 (2), 27–43.

    CAS  Google Scholar 

  38. Vyskocil F., Malomouzh A.I., Nikolsky E.E. 2009. Non-quantal acetylcholine release at the neuromuscular junction. Physiol. Res. 58, 763–784.

    CAS  PubMed  Google Scholar 

  39. Nikolsky E.E., Voronin V.A. 1986. Temperature dependence of the processes of spontaneous quantal and nonquantal release of transmitter from motor nerve endings of the mouse. Neirofiziologiya (Rus.). 18, 361–367.

    Google Scholar 

  40. Lupa M.T., Tabti N., Thesleff S., Vyskocil F., Yu S.P. 1986. The nature and origin of calcium-insensitive miniature end-plate potentials at rodent neuromuscular junctions. J. Physiol. 381, 607–618.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Giniatullin R.A., Khazipov R.N., Oranska T.I., Nikolsky E.E., Voronin V.A., Vyskocil F. 1993. The effect of non-quantal acetylcholine release on quantal miniature currents at mouse diaphragm. J. Physiol. 466, 105–114.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Barrett E.F., Barrett J.N., Botz D., Chang D.B., Mahaffey D. 1978. Temperature-sensitive aspects of evoked and spontaneous transmitter release at the frog neuromuscular junction. J. Physiol. 279, 253–273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Glavinovic M.I. 1979. Voltage clamping of unparalysed cut rat diaphragm for study of transmitter release. J. Physiol. 290 (2), 467–480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Katz B., Miledi R. 1965. The effect of temperature on the synaptic delay at the neuromuscular junction. J. Physiol. 181 (3), 656–670.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Barrett E.F., Stevens C.F. 1972. The kinetics of transmitter release at the frog neuromuscular junction. J. Physiol. 227 (3), 691–708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Datyner N.B., Gage P.W. 1980. Phasic secretion of acetylcholine at a mammalian neuromuscular junction. J. Physiol. 303, 299–314.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Moyer M., van Lunteren E. 2001. Effect of temperature on endplate potential rundown and recovery in rat diaphragm. J. Neurophysiol. 85 (5), 2070–2075.

    CAS  PubMed  Google Scholar 

  48. Barrnett R.J. 1962. The fine structural localization of acetylcholinesterase at the myoneural junction. J. Cell. Biol. 12, 247–262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Foldes F.F., Kuze S., Vizi E.S., Deery A. 1978. The influence of temperature on neuromuscular performance. J. Neural. Transm. 43 (1), 27–45.

    Article  CAS  PubMed  Google Scholar 

  50. Kordas M. 1972. An attempt at an analysis of the factors determining the time course of the end-plate current. II. Temperature. J. Physiol. 224 (2), 333–348.

    CAS  PubMed  Google Scholar 

  51. Nikolsky E.E., Strunsky E.G., Vyskocil F. 1991. Temperature dependence of carbachol-induced modulation of miniature end-plate potential frequency in rats. Brain Res. 560 (1–2), 354–356.

    Article  CAS  PubMed  Google Scholar 

  52. Kochubey P.V., Bershitsky S.Yu. 2014. Comparison of the force and rate of contraction of fast- and slowtwitch skeletal muscle fibers of the rabbit at different temperatures. Biofizika (Rus.). 59 (5), 967–972.

    Google Scholar 

  53. Volkov E.M., Valiullin V.V. 1985. Effect of thyroxin on the properties of skeletal muscle fibers of the frog. Fiziol. Zh. SSSR (Rus.). 71 (9), 1082–1087.

    CAS  Google Scholar 

  54. Asmussen G., Beckers-Bleukx G., Maréchal G. 1994. The force-velocity relation of the rabbit inferior oblique muscle; Influence of temperature. Pflügers Arch. 426 (6), 542–547.

    Article  CAS  PubMed  Google Scholar 

  55. Asmussen G., Maréchal G. 1989. Maximal shortening velocities, isomyosins and fibre types in soleus muscle of mice, rats and guinea-pigs. J. Physiol. 416, 245–254.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Barclay C.J., Constable J.K., Gibbs C.L. 1993. Energetics of fast- and slow-twitch muscles of the mouse. J. Physiol. 472, 61–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Leijendekker W.J., Elzinga G. 1990. Metabolic recovery of mouse extensor digitorum longus and soleus muscle. Pflügers Arch. 416 (1–2), 22–27.

    Article  CAS  PubMed  Google Scholar 

  58. Petrofsky J.S., Lind A.R. 1981. The influence of temperature on the isometric characteristics of fast and slow muscle in the cat. Pflügers Arch. 389 (2), 149–154.

    Article  CAS  PubMed  Google Scholar 

  59. Kössler F., Küchler G. 1987. Contractile properties of fast and slow twitch muscles of the rat at temperatures between 6 and 42°C. Biomed. Biochim. Acta. 46 (11), 815–822.

    PubMed  Google Scholar 

  60. Gilliver S.F., Jones D.A., Rittweger J., Degens H. 2011. Variation in the determinants of power of chemically skinned type I rat soleus muscle fibres. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 197 (4), 311–319.

    Article  PubMed  Google Scholar 

  61. Binkhorst R.A., Hoofd L., Vissers A.C. 1977. Temperature and force-velocity relationship of human muscles. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 42 (4), 471–475.

    CAS  PubMed  Google Scholar 

  62. Bottinelli R., Canepari M., Pellegrino M.A., Reggiani C. 1996. Force-velocity properties of human skeletal muscle fibres: Myosin heavy chain isoform and temperature dependence. J. Physiol. 495 (Pt 2), 573–586.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Buller A.J., Kean C.J., Ranatunga K.W., Smith J.M. 1984. Temperature dependence of isometric contractions of cat fast and slow skeletal muscles. J. Physiol. 355, 25–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Candau R., Iorga B., Travers F., Barman T., Lionne C. 2003. At physiological temperatures the ATPase rates of shortening soleus and psoas myofibrils are similar. Biophys. J. 85 (5), 3132–3141.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Bennett A.F. 1984. Thermal dependence of muscle function. Am. J. Physiol. 247 (2 Pt 2), R217–229.

    CAS  PubMed  Google Scholar 

  66. Gulati J. 1976. Force-velocity characteristics for calcium- activated mammalian slow-twitch and fasttwitch skeletal fibers from the guinea pig. Proc. Natl. Acad. Sci. USA. 73 (12), 4693–4697.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Claflin D.R., Faulkner J.A. 1989. The force-velocity relationship at high shortening velocities in the soleus muscle of the rat. J. Physiol. 411, 627–637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Goldman Y.E., McCray J.A., Ranatunga K.W. 1987. Transient tension changes initiated by laser temperature jumps in rabbit psoas muscle fibres. J. Physiol. 392, 71–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Rossi R., Maffei M., Bottinelli R., Canepari M. 2005. Temperature dependence of speed of actin filaments propelled by slow and fast skeletal myosin isoforms. J. Appl. Physiol. 99 (6), 2239–2245.

    Article  CAS  PubMed  Google Scholar 

  70. Sabelli H.C., Mosnaim A.D., Vazquez A.J., Giardina W.J., Borison R.L., Pedemonte W.A. 1976. Biochemical plasticity of synaptic transmission: A critical review of Dale’s principle. Biol. Psychiatry. 11 (4), 481–524.

    CAS  PubMed  Google Scholar 

  71. Mukhamedyarov M.A., Grishin S.N., Zefirov A.L., Palotas A. 2009. The mechanisms of multi-component paired-pulse facilitation of neurotransmitter release at the frog neuromuscular junction. Pflügers Arch. 458 (3), 563–570.

    Article  CAS  PubMed  Google Scholar 

  72. Grishin S.N. 2014. Transmembrane calcium current: Mechanism, registration procedures, and Ca2+-mediated modulators of synaptic transmission. Biochem. (Mosc.) Suppl. Series A: Membrane and Cell Biology. 8 (3), 213–224.

    Article  Google Scholar 

  73. Grishin S.N. 2016. Neuromuscular transmission in the absence of calcium in extracellular medium. Biol. Membrany (Rus.). 33 (2), 87–97.

    CAS  Google Scholar 

  74. Rich T.L., Langer G.A. 1976. Effects of calcium-free perfusion on excitation-contraction coupling in heart and skeletal muscle. Recent. Adv. Stud. Cardiac. Struct. Metab. 9, 95–100.

    CAS  PubMed  Google Scholar 

  75. Stephenson D.G., Williams D.A. 1981. Calcium-activated force responses in fast- and slow-twitch skinned muscle fibres of the rat at different temperatures. J. Physiol. 317, 281–302.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Burnstock G., Arnett T.R., Orriss I.R. 2013. Purinergic signalling in the musculoskeletal system. Purinergic Signal. 9 (4), 541–572.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Grishin S.N., Ziganshin A.U. 2013. Modulatory role of purines in neuromuscular transmission. Biochemistry (Moscow). 7 (3), 183–191.

    Google Scholar 

  78. Ziganshin A.U., Kamaliev R.R., Grishin S.N., Ziganshin B.A., Burnstock G. 2009. Interaction of hydrocortisone with ATP and adenosine on nerve-mediated contractions of frog skeletal muscle. Eur. J. Pharmacol. 607, 54–59.

    Article  CAS  PubMed  Google Scholar 

  79. Saitongdee P., Becker D.L., Milner P., Knight G.E., Burnstock G. 2004. Levels of gap junction proteins in coronary arterioles and aorta of hamsters exposed to the cold and during hibernation and arousal. J. Histochem. Cytochem. 52 (5), 603–615.

    Article  CAS  PubMed  Google Scholar 

  80. Wallace A., Knight G.E., Cowen T., Burnstock G. 2006. Changes in purinergic signalling in developing and ageing rat tail artery: Importance for temperature control. Neuropharmacology. 50 (2), 191–208.

    Article  CAS  PubMed  Google Scholar 

  81. Ziganshin A.U., Rychkov A.V., Ziganshina L.E., Burnstock G. 2002. Temperature dependency of P2 receptor- mediated responses. Eur. J. Pharmacol. 456 (1–3), 107–114.

    Article  CAS  PubMed  Google Scholar 

  82. Ziganshin A.U., Kamaliev R.R., Grishin S.N., Ziganshina L.E., Zefirov A.L., Burnstock G. 2005. The influence of hypothermia on P2 receptor-mediated responses of frog skeletal muscle. Eur. J. Pharmacol. 21, 187–193.

    Article  Google Scholar 

  83. Ziganshin A.U., Khairullin A.E., Zobov V.V., Ziganshina L.E., Gabdrakhmanov A.I., Ziganshin B.A., Grishin S.N. 2016. Effects of ATP and adenosine on contraction amplitude of rat soleus muscle at different temperatures. Muscle Nerve. doi 10.1002/mus.25263

  84. Arkhipova O.V., Grishin S.N., Sitdikova G.F., Zefirov A.L. 2006. The presynaptic effects of arachidonic acid and prostaglandin E2 at the frog neuromuscular junction. Neurosci. Behav. Physiol. 36 (3), 307–312.

    Article  CAS  PubMed  Google Scholar 

  85. Doi Y. 1920. Studies on muscular contraction: I. The influence of temperature on the mechanical performance of skeletal and heart muscle. J. Physiol. 54 (4), 218–226.

    CAS  PubMed  Google Scholar 

  86. Rutkove S.B., Kothari M.J., Shefner J.M. 1997. Nerve, muscle, and neuromuscular junction electrophysiology at high temperature. Muscle Nerve. 20 (4), 431–436.

    Article  CAS  PubMed  Google Scholar 

  87. Ferretti G. 1992. Cold and muscle performance. Int. J. Sports Med. 13 (Suppl. 1), S185–S187.

    Article  PubMed  Google Scholar 

  88. Cowan K.J., Storey K.B. 2001.Freeze-thaw effects on metabolic enzymes in wood frog organs. Cryobiology. 43 (1), 32–45.

  89. MacDonald J.A., Storey K.B. 2002. Protein phosphatase type-1 from skeletal muscle of the freeze-tolerant wood frog. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 131 (1), 27–36.

    Article  PubMed  Google Scholar 

  90. Boutilier R.G., St-Pierre J. 2002. Adaptive plasticity of skeletal muscle energetics in hibernating frogs: Mitochondrial proton leak during metabolic depression. J. Exp. Biol. 205 (Pt 15), 2287–2296.

    CAS  PubMed  Google Scholar 

  91. Mantovani M., Heglund N.C., Cavagna G.A. 2001. Energy transfer during stress relaxation of contracting frog muscle fibres. J. Physiol. 537 (Pt 3), 923–939.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Nyitrai M., Rossi R., Adamek N., Pellegrino M.A., Bottinelli R., Geeves M.A. 2006. What limits the velocity of fast-skeletal muscle contraction in mammals? J. Mol. Biol. 355 (3), 432–442.

    Article  CAS  Google Scholar 

  93. Islamov R.R., Kiyasov A.P., Valiullin V.V. 1992. Effect of hypothermia on the development of ischemic injuries to rat skeletal muscle. Byull. Exp. Biol. Med. (Rus.). 113 (1), 92–94.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. N. Grishin.

Additional information

Original Russian Text © A.E. Khairullin, A.U. Ziganshin, S.N. Grishin, 2016, published in Biologicheskie Membrany, 2016, Vol. 33, No. 5, pp. 315–322.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khairullin, A.E., Ziganshin, A.U. & Grishin, S.N. Motor units at various temperatures. Biochem. Moscow Suppl. Ser. A 11, 1–7 (2017). https://doi.org/10.1134/S1990747816040048

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990747816040048

Keywords

Navigation