Linear Electrical Properties of the Transverse Tubules and Surface Membrane of Skeletal Muscle Fibers
01 Nov 1970-The Journal of General Physiology (The Rockefeller University Press)-Vol. 56, Iss: 5, pp 640-671
TL;DR: With the use of two intracellular microelectrodes and a circuit designed to compensate for the effects of stray capacitances around the electrodes, transfer impedance measurements were made on frog sartorius muscle fibers bathed in 7.5 mM K Ringer solution and showed that the fibers behaved as ideal one-dimensional cables having purely resistive internal impedances.
Abstract: With the use of two intracellular microelectrodes and a circuit designed to compensate for the effects of stray capacitances around the electrodes, transfer impedance measurements were made at frequencies from 05 to 1000 c/s on frog sartorius muscle fibers bathed in 75 mM K Ringer solution Complete AC cable analyses performed at 46, 100, 215, 464, and 1000 c/s showed that the fibers behaved as ideal one-dimensional cables having purely resistive internal impedances (Ri = 102 ± 11 Ω cm) Two circuits were considered for fiber inside-outside impedance, a four lumped parameter circuit and a parallel resistance and capacitance shunted by the input impedance of a lattice model for the T-system Least squares fits to fiber input impedance phase angles were better with the latter circuit than with the former With the use of the lattice model the specific capacitance of both the surface and transverse tubule membranes was found to be 1 µF/cm2 and the internal resistivity of the tubules to be about 300 Ω cm
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TL;DR: It is suggested that a link in excitation-contraction coupling involves the movement of a fixed amount of charge free to move between different locations across the membrane.
Abstract: It is suggested that a link in excitation-contraction coupling involves the movement of a fixed amount of charge free to move between different locations across the membrane.
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Cites background from "Linear Electrical Properties of the..."
...Schneider (1970) found that his measurements of input impedance could be reconciled with a similar model if the resistivity of the T lumen was two or three times greater than that of the extracellular solution, and this was interpreted later as greater tortuosity in the network (Mathias et al., 1977); using a twofold greater tortuosity in the calculation of the space constant for radial decay of voltage, the maximum voltage inhomogene-...
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382 citations
TL;DR: Comparison of recorded currents with simulations shows that while the transverse tubular system has regenerative sodium currents, they are too small to make important errors in the total current recorded at the surface under voltage clamp at low temperature.
Abstract: A Vaseline gap potentiometric recording and voltage clamp method is developed for frog skeletal muscle fibers. The method is based on the Frankenhaeuser-Dodge voltage clamp for myelinated nerve with modifications to improve the frequency response, to compensate for external series resistance, and to compensate for the complex impedance of the current-passing pathway. Fragments of single muscle fibers are plucked from the semitendinosus muscle and mounted while depolarized by a solution like CsF. After Vaseline seals are formed between fluid pools, the fiber ends are cut once again, the central region is rinsed with Ringer solution, and the feedback amplifiers are turned on. Errors in the potential and current records are assessed by direct measurements with microelectrodes. The passive properties of the preparation are simulated by the "disk" equivalent circuit for the transverse tubular system and the derived parameters are similar to previous measurements with microelectrodes. Action potentials at 5 degrees C are long because of the absence of delayed rectification. Their shape is approximately simulated by solving the disk model with sodium permeability in the surface and tubular membranes. Voltage clamp currents consist primarily of capacity currents and sodium currents. The peak inward sodium current density at 5 degrees C is 3.7 mA/cm2. At 5 degrees C the sodium currents are smoothly graded with increasing depolarization and free of notches suggesting good control of the surface membrane. At higher temperatures a small, late extra inward current appears for small depolarizations that has the properties expected for excitation in the transverse tubular system. Comparison of recorded currents with simulations shows that while the transverse tubular system has regenerative sodium currents, they are too small to make important errors in the total current recorded at the surface under voltage clamp at low temperature. The tubules are definitely not under voltage clamp control.
310 citations
Cites methods or result from "Linear Electrical Properties of the..."
...The observations on capacity transients were interpreted in terms of a model given by Falk and Fatt (1964) and applied by Adrian et al. (1969), Schneider (1970), and others to the passive electrical properties of the transverse tubular system of muscle....
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...However, our measurements are neither as extensive nor as careful as those of other authors (e.g., Schneider, 1970; Hodgkin and Nakajima, 1972 a,b; Valdiosera et al., 1974)....
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TL;DR: Propagated action potentials of striated muscle are calculated using an equivalent circuit that represents the transverse tubular system as a radial cable of sixteen elements.
Abstract: 1. Propagated action potentials of striated muscle are calculated using an equivalent circuit that represents the transverse tubular system as a radial cable of sixteen elements. The membrane of the transverse tubules is assumed to have activatable ionic currents similar to those in the fibre surface.2. The configuration of the after-potential and the conduction velocity are best accounted for by postulating a resistance of about 150Omega cm(2) separating the extracellular fluid from the lumen of the transverse tubules at the edge of the fibre, and a density of sodium channels in the tubular wall about a twentieth of that in the fibre surface.3. Calculations with imposed voltage steps at the fibre surface suggest that the potential across the tubular membrane at the centre of the fibre is very far from clamped.4. Currents providing charge for the tubular capacity can give rise to substantial errors in estimating the zero-current potential of the ionic currents.
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TL;DR: The most widely accepted theory of the restirng potential of muscle is that the electrical potential difference between the inside and outside of a muscle fibre arises from the concentration gradients of the potassium and chloride ions.
Abstract: The most widely accepted theory of the restirng potential of muscle is that the electrical potential difference between the inside and outside of a muscle fibre arises from the concentration gradients of the potassium and chloride ions. If we follow Boyle & Conway (1941), the membrane is assumed to be permeable to K and Cl but to be impermeable or sparingly permeable to other ions. Since K is more concentrated inside and Cl is more concentrated outside, the interior of the fibre should be electrically negative to the external solution. If K and Cl are distributed passively, the concentration ratios and the membrane potential under equilibrium conditions ought to conform to the relation
1,392 citations
TL;DR: The buffers described in this section are suitable for use either in enzymatic or histochemical studies, and the titration curves of the majority of the buffers recommended have been redetermined by the writer.
Abstract: The methods of preparation described are not necessarily identical with those of the original authors. The titration curves of the majority of the buffers recommended have been redetermined by the writer. The buffers are arranged in the order of ascending pH range. For more complete data on phosphate and acetate buffers over a wide range of concentrations, see Vol. I [10].*
1,163 citations
"Linear Electrical Properties of the..." refers methods in this paper
...Experiments were carried out on sartorius muscles of Rana pipiens at 24-26 0 C in a solution (7.5 m K Ringer) containing 115 mM NaC1, 7.5 mM KC1, 1.8 mM CaCI 2 , and 1 mM tris (hydroxymethyl) aminomethane maleate buffer (Gomory, 1955), pH 7.1....
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...8 mM CaCI2, and 1 mM tris (hydroxymethyl) aminomethane maleate buffer (Gomory, 1955), pH 7....
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952 citations
TL;DR: The sarcoplasmic reticulum of the frog's sartorius muscle was examined by electron microscopy following sequential fixation in glutaraldehyde and osmium tetroxide and embedding in Epon, finding evidence for continuity of the transverse tubules with the fiber surface.
Abstract: The sarcoplasmic reticulum of the frog's sartorius muscle was examined by electron microscopy following sequential fixation in glutaraldehyde and osmium tetroxide and embedding in Epon. The earlier results of Porter and Palade on Ambystoma muscle were confirmed in the sartorius. In addition, the transverse tubules were observed to be continuous across the width of the fiber, a set of flat intermediate cisternae was seen to connect the terminal cisternae to the longitudinal tubules in the A band, and the continuous reticulum collar at the center of the A band was found to be perforated by circular and elongated pores (the fenestrated collar). The transverse tubules have a volume about 0.3 per cent of the fiber volume, and a surface area about 7 times the outer cylindrical surface area for a fiber 100 micro in diameter. The terminal cisternae, the intermediate cisternae, and the longitudinal tubules together with the fenestrated collar each have a volume of 4 to 5 per cent of the fiber volume and a surface area 40 to 50 times the outer surface area of a fiber 100 micro in diameter. Some evidence for continuity of the transverse tubules with the fiber surface is presented, but this is thought to be not so convincing as evidence presented by others. The results are discussed in terms of a possible mechanism for a role of the transverse tubules and sarcoplasmic reticulum in excitation-contraction coupling, as suggested by their morphology and a variety of physiological studies. In this scheme, the transverse tubules are thought to be electrically coupled to the terminal cisternae, so that depolarization of the fiber surface spreads inward along the transverse tubules and to the terminal cisternae, initiating the release of a contraction-activating substance.
622 citations
"Linear Electrical Properties of the..." refers methods in this paper
...…were determined from K 1 , K 2 , and K 4 , respectively, using rearrangements of equations (32) through (34). rc, was calculated using 3.75 A -' (Peachey, 1965) for the length of T-tubule per unit cross-section area in the THE JOURNAL OF GENERAL PHYSIOLOGY VOLUME 56 -1970 plane of the lattice…...
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...A T-tubule perimeter of 0.2 /A (Peachey, 1965) was used to refer r. and c to a unit area of tubule membrane giving R, and C., and a crosssection area/of 2 X 1 0- 3 /u 2 (Peachey, 1965) used to convert rl to the specific resistivity R 1 of the tubule contents....
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...With the use of the structural data presented by Peachey (1965), both tubule and surface membranes were found to have specific capacitances close to 1 4uF/cm 2 ....
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471 citations