Skip to main content
Log in

Passive electrical properties and voltage dependent membrane capacitance of single skeletal muscle fibers

  • Excitable Tissues and Central Nervous Physiology
  • Published:
Pflügers Archiv Aims and scope Submit manuscript

Abstract

The passive membrane capacitance and conductance of isolated single muscle fibers were investigated using a vaseline gap method. The results obtained with this method are consistent with those obtained using the microelectrode technique. It was confirmed that the membrane capacitance of skeletal muscle consisted of a large capacitance of tubular membrane (7–10 μF/cm2) and a much smaller capacitance of surface membrane (1–2 μF/cm2). The relative time constants of these two components vary from one sample to another, resulting in one time and two time constant behaviors.

Secondly, the capacitance of isolated skeletal muscle fibers was investigated during hyper- and depolarizing pulses, using the transient bridge technique with the vaseline gap method. Measurements were performed at two frequencies, i.e. 500 Hz and 20 kHz. It was found that the membrane capacitance increased by 15–20% with depolarizations. The voltage dependent membrane capacitance was no affected by the addition of tetrodotoxin in bathing solution blocking sodium current and muscle contraction. Also, blocking both Na and K current did not have an appreciable effect on the non-linear behavior of membrane capacitance. The origin of voltage dependent capacitance in muscle membrane appears to be distributed among several non-linear ionic processes such as Na and K currents and the flux of Ca and Cl ions and their accumulation.

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

  • Adrian RH, Almers W (1976a) The voltage dependence of membrane capacity. J Physiol (Lond) 254:317–338

    Google Scholar 

  • Adrian RH, Almers W (1976b) Charge movement in the membrane of striated muscle. J Physiol (Lond), 254:339–360

    Google Scholar 

  • Almers W (1978) Gating currents and charge movements in excitable membranes. Rev Physiol Biochem Pharmacol 82:96–190

    Google Scholar 

  • Armstrong CM, Bezanilla F (1973) Currents related to movement of the gating particles of the sodium channels. Nature (Lond) 242:459–461

    Google Scholar 

  • Armstrong CM, Bezanilla F (1974) Charge movement associated with the opening and closing of the activation gates of the Na channels. J Gen Physiol 63:533–552

    Google Scholar 

  • Ashcroft FM, Stanfield PR (1981) Calcium dependence of the inactivation of calcium currents in skeletal muscle fibers of an insect. Science 213:224–226

    Google Scholar 

  • Campbell DT (1983) Sodium channel gating currents in frog skeletal muscle. J Gen Physiol 82:679–701

    Google Scholar 

  • Eisenberg RS, Gage PW (1967) Frog skeletal muscle fibers; changes in electrical properties after disruption of transverse tubular system. Science 158:1700–1701

    Google Scholar 

  • Eisenberg B, Eisenberg RS (1968) Selective disruption of the sacrotubular system in frog sartorius muscle. J Cell Biology 39: 451–467

    Google Scholar 

  • Falk G, Fatt P (1964) Linear electrical properties of striated muscle fibers observed with intracellular electrodes. Proc Roy Soc Ser B 160:69–123

    Google Scholar 

  • Fernandez JM, Bezanilla F, Taylor RE (1982) Distribution and kinetics of membrane dielectric polarization. J Gen Physiol 79:41–67

    Google Scholar 

  • Fishman HM, Moore LE, Poussart D, Leuchtag HR, Sanchez J (1977) No capacitance increase in squid axon admittance when “inactivation” of “gating charge” is insufficient. Biophys J 33: 281a

    Google Scholar 

  • Freygang WH, Jr, Rapopport SI, Peachey LD (1967) Some relations between changes in the linear electrical properties of striated muscle fibers and changes in ultrastructure. J Gen Physiol 50:2437–2458

    Google Scholar 

  • Gage PW, Eisenberg RS (1969a) Capacitance of the surface and transverse tubular membrane of frog sartorius fibers. J Gen Physiol 59:347–359

    Google Scholar 

  • Gage PW, Eisenberg RS (1969b) Action potentials, afterpotentials and excitation-contraction coupling in frog sartorious fibers without transverse tubules. J Gen Physiol 56:640–671

    Google Scholar 

  • Guttman R (1939) The electrical impedance of muscle during the action of narcotics and other agents. J Gen Physiol 22:567–591

    Google Scholar 

  • Hille B, Cambell DT (1976) An improved vaseline gap voltage clamp for skeletal muscle fibers. J Gen Physiol 67:265–293

    Google Scholar 

  • Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol (Lond) 117:500–544

    Google Scholar 

  • Hodgkin AL, Nakajima S (1972) The effect of diameter on the electrical constants of skeletal frog muscle fibers. J Physiol 221:105–120

    Google Scholar 

  • Horowicz P, Schneider MF (1981) Membrane charge movement in contracting and non-contracting skeletal muscle fibers. J Physiol 314:565–593

    Google Scholar 

  • Huang CLH (1981a) Dielectric components of charge movements in skeletal muscle. J Physiol 313:187–205

    Google Scholar 

  • Huang CLH (1981b) Membrane capacitance in hyperpolarized muscle fibers. J Physiol 313:206–222

    Google Scholar 

  • Keynes RD, Rojas E (1976) Kinetics and steady-state properties of the system controlling sodium conductance in the squid giant axon. J Physiol 239:393–434

    Google Scholar 

  • Meves H (1976) The effect of molding potential on the asymmetry currents in squid giant axons. J Physiol 254:787–801

    Google Scholar 

  • Meves H (1977) Activation, inactivation and chemical blockade of the gating current in squid giant axons. Ann NY Acad Sci 303:321–388

    Google Scholar 

  • Schneider MF, Chandler WK (1973) Voltage-dependent charge movement in skeletal muscle: A possible step in excitation-contraction coupling. Nature (Lond) 242:244–246

    Google Scholar 

  • Schneider MF, Chandler WK (1976) Effects of membrane potential on the capacitance of skeletal muscle fibers. J Physiol 67:125–163

    Google Scholar 

  • Schwan HP (1954) Die elektrischen Eigenschaften von Muskelgewebe bei Niederfrequenz. A Naturforsch 9b:245–251

    Google Scholar 

  • Takashima S (1978) Frequency domain analysis of asymmetry current in squid axon membrane. Biophys J 22:115–119

    Google Scholar 

  • Takashima S, Yantorno R (1977) Investigation of voltage-dependent membrane capacity of squid giant axons. Ann NY Acad Sci 303:306–321

    Google Scholar 

  • Takashima S, Schwan HP (1974) Passive electrical properties of squid axon membrane. J Membrane Biol 17:51–68

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takashima, S. Passive electrical properties and voltage dependent membrane capacitance of single skeletal muscle fibers. Pflugers Arch. 403, 197–204 (1985). https://doi.org/10.1007/BF00584100

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00584100

Key words

Navigation