Skip to main content
SpringerLink
Log in

Effect of repetitive stimulation on cell volume and its relationship to membrane potential in amphibian skeletal muscle

  • Skeletal Muscle
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

The effect of electrical stimulation on cell volume, V c, and its relationship to membrane potential, E m, was investigated in Rana temporaria striated muscle. Confocal microscope xz-plane scanning and histology of plastic sections independently demonstrated significant and reversible increases in V c of 19.8±0.62% (n=3) and 27.1±8.62% (n=3), respectively, after a standard stimulation protocol. Microelectrode measurements demonstrated an accompanying membrane potential change, ΔE m, of +23.6±0.98 mV (n=3). The extent to which this ΔE m might contribute to the observed changes in V c was explored in quiescent muscle exposed to variations in extracellular potassium concentration, [K+]e. E m and V c varied linearly with log [K+]e and [K+]e, respectively, in the range 2.5–15 mM (R 2=0.99 and 0.96), and these results were used to reconstruct an approximately linear relationship between V c and E m (ΔV c=0.85E m+68.53; R 2=0.99) and hence derive the ΔV c expected from the ΔE m during stimulation. This demonstrated that both the time course and magnitude of the increase and recovery of V c observed in active muscles could be reproduced by the corresponding [K+]e-induced depolarisation in quiescent muscles, suggesting that the depolarisation associated with membrane activity makes a substantial contribution to the cell swelling during exercise. Furthermore, conditions of Cl− deprivation abolished the relationship between E m and V c, supporting a mechanism in which the depolarisation of E m drives a passive redistribution of Cl− and hence cellular entry of Cl− and K+ and an accompanying, osmotically driven, increase in V c.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Adrian RH (1956) The effect of internal and external potassium concentration on the membrane potential of frog muscle. J Physiol 133:631–658

    PubMed  CAS  Google Scholar 

  2. Adrian RH (1960) Potassium chloride movement and the membrane potential of frog muscle. J Physiol 151:154–185

    PubMed  CAS  Google Scholar 

  3. Balog EM, Fitts RH (1996) Effects of fatiguing stimulation on intracellular Na+ and K+ in frog skeletal muscle. J Appl Physiol 81:679–685

    PubMed  CAS  Google Scholar 

  4. Blinks JR (1965) Influence of osmotic strength on cross-section and volume of isolated single muscle fibres. J Physiol 177:42–57

    PubMed  CAS  Google Scholar 

  5. Boyle PJ, Conway EJ (1941) Potassium accumulation in muscle and associated changes. J Physiol 100:1–63

    PubMed  CAS  Google Scholar 

  6. Creese R, Hashish SEE, Scholes NW (1958) Potassium movements in contracting diaphragm muscle. J Physiol 143:307–324

    PubMed  CAS  Google Scholar 

  7. Donaldson PJ, Leader JP (1984) Intracellular ionic activities in the EDL muscle of the mouse. Pflugers Arch 400:166–170

    Article  PubMed  CAS  Google Scholar 

  8. Eisenberg BR, Gilai A (1979) Structural changes in single muscle fibres after stimulation at a low frequency. J Gen Physiol 74:1–16

    Article  PubMed  CAS  Google Scholar 

  9. Ferenczi EA, Fraser JA, Chawla C, Skepper JN, Schwiening CJ, Huang CL-H (2004) Membrane potential stabilization in amphibian skeletal muscle fibres in hypertonic solutions. J Physiol 555:423–438

    Article  PubMed  CAS  Google Scholar 

  10. Fisher MJ, Meyer RA, Adams GR, Foley JM, Potchen EJ (1990) Direct relationship between proton T2 and exercise intensity in skeletal muscle MR images. Invest Radiol 25:480–485

    Article  PubMed  CAS  Google Scholar 

  11. Fraser JA, Huang CL-H (2004) A quantitative analysis of cell volume and resting potential determination and regulation in excitable cells. J Physiol 559:459–478

    Article  PubMed  CAS  Google Scholar 

  12. Fraser JA, Skepper JN, Hockaday AR, Huang CL (1998) The tubular vacuolation process in amphibian skeletal muscle. J Muscle Res Cell Motil 19:613–629

    Article  PubMed  CAS  Google Scholar 

  13. Fraser JA, Middlebrook CE, Usher-Smith JA, Schwiening CJ, Huang CL-H (2005) The effect of intracellular acidification on the relationship between cell volume and membrane potential in amphibian skeletal muscle. J Physiol 563:745–764

    Article  PubMed  CAS  Google Scholar 

  14. Fraser JA, Rang CE, Usher-Smith JA, Huang CL-H (2005) Slow volume transients in amphibian skeletal muscle fibres studied in hypotonic solutions. J Physiol 564:51–63

    Article  PubMed  CAS  Google Scholar 

  15. Gallagher FA, Huang CL (1997) Osmotic ‘detubulation’ in frog muscle arises from a reversible vacuolation process. J Muscle Res Cell Motil 18:305–321

    Article  PubMed  CAS  Google Scholar 

  16. Geukes Foppen RJ (2004) In skeletal muscle the relaxation of the resting membrane potential induced by K+ permeability changes depends on Cl− transport. Pflugers Arch 447:416–425

    Article  PubMed  CAS  Google Scholar 

  17. Geukes Foppen RJ, van Mil HGJ, Siegenbeek van Heukelom J (2002) Effects of chloride transport on bistable behaviour of the membrane potential in mouse skeletal muscle. J Physiol 542:181–191

    Article  PubMed  CAS  Google Scholar 

  18. Green S, Langberg H, Skovgaard D, Bulow J, Kjaer M (2000) Interstitial and arterial-venous [K+] in human calf muscle during dynamic exercise: effect of ischaemia and relation to muscle pain. J Physiol 529:849–861

    Article  PubMed  CAS  Google Scholar 

  19. Hallen J, Gullestad L, Sejersted OM (1994) K+ shifts of skeletal muscle during stepwise bicycle exercise with and without beta-adrenoceptor blockade. J Physiol 477:149–159

    PubMed  CAS  Google Scholar 

  20. Hill AV, Kupalov P (1929) Anaerobic and aerobic activity in isolated muscle. Proc R Soc Lond B Biol Sci 105:313

    Article  CAS  Google Scholar 

  21. Hnik P, Holas M, Krekule I, Kuriz N, Mejsnar J, Smiesko V, Ujec E, Vyskocil F (1976) Work-induced potassium changes in skeletal muscle and effluent venous blood assessed by liquid ion-exchanger microelectrodes. Pflugers Arch 362:85–94

    Article  PubMed  CAS  Google Scholar 

  22. Hodgkin AL, Horowicz P (1960) The effect of sudden changes in ionic concentrations on the membrane potential of single muscle fibres. J Physiol 153:370–385

    PubMed  CAS  Google Scholar 

  23. Hutter OF, Noble D (1960) The chloride conductance of frog skeletal muscle. J Physiol 151:89–102

    PubMed  CAS  Google Scholar 

  24. Hutter OF, Padsha SM (1959) Effect of nitrate and other anions on the membrane resistance of frog skeletal muscle. J Physiol 146(1):117–132

    PubMed  CAS  Google Scholar 

  25. Juel C (1986) Potassium and sodium shifts during in vitro isometric muscle contraction, and the time course of the ion-gradient recovery. Pflugers Arch 406:458–463

    Article  PubMed  CAS  Google Scholar 

  26. Juel C (1988) Muscle pH regulation: role of training. Acta Physiol Scand 162:359–366

    Article  Google Scholar 

  27. Juel C, Pilegaard H, Nielsen JJ, Bangsbo J (2000) Interstitial K(+) in human skeletal muscle during and after dynamic graded exercise determined by microdialysis. Am J Physiol Regul Integr Comp Physiol 278:R400–R406

    PubMed  CAS  Google Scholar 

  28. Krause U, Wegener G (1991) Metabolic changes in skeletal muscle of frog during exercise and recovery. Biochem Soc Trans 19:137S

    PubMed  CAS  Google Scholar 

  29. Lang F, Busch GL, Volkl H (1998) The diversity of volume regulatory mechanisms. Cell Physiol Biochem 8:1–45

    Article  PubMed  CAS  Google Scholar 

  30. Lannergren J (1990) Volume changes of isolated Xenopus muscle fibres associated with repeated tetanic contractions. J Physiol 420:116P

    Google Scholar 

  31. Launikonis BS, Stephenson DG (2002) Tubular system volume changes in twitch fibres from toad and rat skeletal muscle assessed by confocal microscopy. J Physiol 538:607–618

    Article  PubMed  CAS  Google Scholar 

  32. Lindinger MI, Heigenhauser GJF (1991) The roles of ion fluxes in skeletal muscle fatigue. Can J Physiol Pharmacol 69:246–253

    PubMed  CAS  Google Scholar 

  33. Lundvall J (1972) Tissue hyperosmolality as a mediator of vasodilation and transcapillary fluid flux in exercising skeletal muscle. Acta Physiol Scand Suppl 379:1–142

    PubMed  CAS  Google Scholar 

  34. Peracchia C, Mittler BS (1972) Fixation by means of glutaraldehyde-hydrogen peroxide reaction products. J Cell Biol 53(1):234–238

    Article  PubMed  CAS  Google Scholar 

  35. Ploutz-Snyder LL, Convertino VA, Dudley GA (1995) Resistance exercise induced fluid shifts: change in active muscle size and plasma volume. Am J Physiol 269:R536–R543

    PubMed  CAS  Google Scholar 

  36. Rapp G, Ashley CC, Bagni MA, Griffiths PJ, Cecchi G (1998) Volume changes of the myosin lattice resulting from repetitive stimulation of single muscle fibres. Biophys J 75:2984–2995

    PubMed  CAS  Google Scholar 

  37. Ruff RL (1996) Sodium channel slow inactivation and the distribution of sodium channels on skeletal muscle fibres enable the performance properties of different skeletal muscle fibres types. Acta Physiol Scand 156:159–168

    Article  PubMed  CAS  Google Scholar 

  38. Sejersted OM, Sjogaard G (2000) Dynamics and consequences of potassium shifs in skeletal muscle and heart during exercise. Physiol Rev 80:1411–1481

    PubMed  CAS  Google Scholar 

  39. Sjogaard G (1983) Electrolytes in slow and fast muscle fibres of humans at rest and with dynamic exercise. Am J Physiol Regul Integr Comp Physiol 245:R25–R31

    CAS  Google Scholar 

  40. Sjogaard G (1990) Exercise-induced muscle fatigue: the significance of potassium. Acta Physiol Scand Suppl 593:1–63

    PubMed  CAS  Google Scholar 

  41. Sjogaard G, Adams RP, Saltin B (1985) Water and ion shifts in skeletal muscle of humans with intense dynamic knee extension. Am J Physiol 248:R190–R196

    PubMed  CAS  Google Scholar 

  42. Vaughan-Jones RD (1982) Chloride activity and its control in skeletal and cardiac muscle. Philos Trans R Soc Lond B Biol Sci 299:537–548

    Article  PubMed  CAS  Google Scholar 

  43. Ward DS, Hamilton MT, Watson PD (1996) Measurement of tissue volume during non-steady state high-intensity muscle contraction. Am J Physiol 271:R1682–R1690

    PubMed  CAS  Google Scholar 

  44. Watson PD, Garner RP, Ward DS (1993) Water uptake in simulated cat skeletal muscle. Am J Physiol 264:R790–R796

    PubMed  CAS  Google Scholar 

  45. Westerblad H, Lannergren J (1986) Force and membrane potential during and after fatiguing, intermittent tetanic stimulation of single Xenopus muscle fibres. Acta Physiol Scand 128:369–378

    Article  PubMed  CAS  Google Scholar 

  46. Wong JA, Fu L, Schneider EG, Thomason DB (1999) Molecular and functional evidence for Na+-K+-2Cl− cotransporter expression in rat skeletal muscle. Am J Physiol 277:R154–R161

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

C.L.-H.H. thanks the Medical Research Council, the Wellcome Trust and the British Heart Foundation for generous support. J.A.U-S. thanks Astra Zeneca and acknowledges additional support from the James Baird Fund. J.N.S thanks the Wellcome Trust for support, and J.A.F was supported by the George Henry Lewes Fund.

Author information

Authors and Affiliations

  1. Physiological Laboratory, University of Cambridge, Downing Street, Cambridge, CB2 3EG, UK

    Juliet A. Usher-Smith, James A. Fraser & Christopher L.-H. Huang

  2. Multi-Imaging Centre, University of Cambridge, Downing Street, Cambridge, CB2 3EG, UK

    Jeremy N. Skepper

Authors
  1. Juliet A. Usher-Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeremy N. Skepper
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James A. Fraser
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christopher L.-H. Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juliet A. Usher-Smith.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Usher-Smith, J.A., Skepper, J.N., Fraser, J.A. et al. Effect of repetitive stimulation on cell volume and its relationship to membrane potential in amphibian skeletal muscle. Pflugers Arch - Eur J Physiol 452, 231–239 (2006). https://doi.org/10.1007/s00424-005-0022-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-005-0022-9

Keywords

Search

Navigation