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Activation in Striated Muscle

L. L. Costantin

10.1002/cphy.cp010107

Source: Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons

Originally published: 1977

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Structure of Striated Muscle
1.1 Contractile Mechanism
1.2 Internal Membrane System
1.3 Comparative Anatomy of Internal Membrane System
2 Resting Electrical Properties of Skeletal Muscle
2.1 Ionic Permeability
2.2 Resting Electrical Properties of Internal Membrane System
2.3 Detubulated Muscle
3 Excitation in Skeletal Muscle
3.1 Ionic Basis of Action Potential
3.2 Inward Spread of Activation
3.3 T‐system Conductance Changes in Frog Twitch Fibers
4 Excitation‐Contraction Coupling in Skeletal Muscle
4.1 Calcium Activation of Contractile Mechanism
4.2 Calcium Transport and Storage in SR
4.3 Mechanism of Calcium Release
4.4 Role of SR‐T Junction in E‐C Coupling
4.5 Membrane Potential and Contractile Activation
4.6 Time Course of Calcium Release: Calcium Transient
4.7 Contractile Activation Without Membrane Depolarization
4.8 Electrical Events Associated with Activation
4.9 Role of Extracellular Calcium in Contractile Activation
4.10 Calcium‐Sodium Exchange
4.11 Pharmacological Alterations of E‐C Coupling
5 Cellular Organization of Cardiac Muscle
6 Resting Electrical Properties of Cardiac Muscle
6.1 Ionic Permeability
6.2 Membrane Capacity and Resistance
7 Action Potential in Mammalian Cardiac Muscle
7.1 Ionic Basis of Action Potential
8 Voltage‐Clamp Studies of Mammalian Cardiac Muscle
8.1 Purkinje Fiber Preparation
8.2 Outward Currents in Purkinje Cells
8.3 Inward Currents in Purkinje Cells
8.4 Ventricular Myocardial Preparations
8.5 Ionic Currents in Myocardial Preparations
8.6 Ionic Basis of Plateau Potential ‐ Summary
9 Action Potential in Frog Myocardial Cells
10 Voltage‐Clamp Studies of Frog Cardiac Muscle
10.1 Frog Myocardial Preparations
10.2 Ionic Currents in Frog Myocardium
11 E‐C Coupling in Cardiac Muscle
11.1 Calcium Influx and Alterations in SR Calcium Stores
11.2 Calcium Influx and Contractile Activation
Figure 1. Figure 1.

Sarcomere pattern in striated muscle. An electron micrograph of a longitudinal section through 2 myofibrils of a frog skeletal muscle is shown above, and the overlap of thick and thin filaments that gives rise to the pattern of bands within the sarcomere is illustrated schematically below. The 2 myofibrils are separated by elements of the internal membrane system. The I band is light because it consists only of thin filaments. The A band is dark where it consists of overlapping thick and thin filaments and lighter in the H zone where it consists solely of thick filaments. The M line is caused by a bulge in the center of each thick filament and the pseudo H zone by a central region of the thick filament that lacks cross bridges.

From Huxley 187. Copyright © 1965 by Scientific American, Inc. All rights reserved
Figure 2. Figure 2.

Schematic reconstruction of a small portion of a frog twitch muscle fiber. The longitudinal axis of the fiber runs from left to right. The contractile filaments are grouped into roughly cylindrical myofibrils about 1 μm in diameter, and each myofibril is enveloped by the transverse tubular system (T system) and the sarcoplasmic reticulum (SR). The close association among the T tubule and 2 terminal cisternae of the SR to form a triad is seen in section in the lower portion of the figure. The elliptical T tubule is about 250 × 800 A in diameter.

From Peachey 287
Figure 3. Figure 3.

Schematic representation of the organization of the SR in a frog heart fiber. A portion of the cell membrane is shown together with 2 myofibrils and their associated SR tubules. A large proportion of the tubules partially surrounds the myofibrils at Z‐line level; connected with these are others oriented in a roughly longitudinal direction. At the cell periphery branches of the SR tubules terminate, usually at I‐band level, in disklike structures that form junctional contacts with the surface membrane of the cell.

From Page & Niedergerke 286
Figure 4. Figure 4.

Inward rectification in frog skeletal muscle. The relation between membrane potential and membrane current is shown for a fiber that was studied successively in sulfate solutions containing 50, 100, and 50 mM K+. The membrane current is in arbitrary units; outward current is taken as positive.

From Adrian 4
Figure 5. Figure 5.

Asymmetry in the membrane potential response of single muscle fibers produced by sudden changes in extracellular potassium in chloride‐free sulfate solution. A: normal fiber. B: glycerol‐treated fiber. Each fiber had been equilibrated in 40 mM K+; solution changes, to 165 mM K+ and back to 40 mM K+, are indicated by the small downward deflections in the lower traces.

From Nakajima et al. 252
Figure 6. Figure 6.

An equivalent circuit containing 2 time‐constants that represents the frequency‐dependent impedance of a frog muscle fiber.Rm and Cm represent the impedance of the surface membrane, and Re and Ce, which provide a pathway for current flow in parallel with the surface membrane, represent the impedance of the T system.

From Falk 97
Figure 7. Figure 7.

Current‐voltage relations in a voltage‐clamped barnacle muscle fiber. (—) Peak early transient current in response to 300‐ms test pulses; (—) steady‐state current; (•) test pulse applied from a holding potential equal to resting potential (−50 mV); (☆) test pulse preceded by a 136‐ms conditioning depolarization to −22 mV; (○–○) membrane current before activation of the early transient current. The point in the current trace at which each measurement was made is shown in the inset.

From Hagiwara et al. 135
Figure 8. Figure 8.

Local activation of a frog twitch fiber. Polarized light compensated so that the A bands appear dark. The fiber is immersed in, and the pipette is also filled with, Ringer's solution. An electric pulse is applied to the pipette making the interior of its tip go roughly 100 mV negative relative to the surrounding fluid for a period of about 0.5 s. In the upper part the pipette is applied to an A band, and there is no response. In the lower part the pipette is applied to an I band, and during the pulse that I band (and only that I band) shortens. Grid spacing, 10 μm.

From Huxley & Taylor 185
Figure 9. Figure 9.

Radial pattern of contractions in TTX‐treated and TTX‐free fibers. The 2 voltage‐clamp microelectrodes can be seen impaling opposite sides of each fiber. Grid spacing, 10 μm. A: fiber in normal Ringer's solution with 50 μg TTX per 100 ml. The resting striation spacing was 2.5 μm. Suprathreshold depolarization produces shortening of the superficial myofibrils without waves to a striation spacing of 1.58–1.76 μm, whereas the axial myofibrils are thrown into waves at striation spacings of 1.65–1.79 μm. White line traces the pattern of the waves. B: no TTX present. Resting striation spacing was 2.5 μm. Suprathreshold depolarization produces shortening of the axial myofibrils without waves to 1.58–1.77 μm, whereas the superficial myofibrils are wavy at striation spacings of 1.90–2.00 μm. White lines trace the pattern of the waves.

From Costantin & Taylor 64
Figure 10. Figure 10.

Late afterpotential following trains of action potentials in a frog twitch fiber. Time course of the membrane potential is displayed at 2 different amplifications and 2 different sweep speeds in the 2 traces of each panel. The gain is 4 times greater for the upper trace, and the time scale of 1 s refers to the upper trace. Action potentials are 10 ms apart. The early afterpotential that follows a single impulse can be seen in the lower right panel.

From Freygang et al. 119
Figure 11. Figure 11.

Action potentials in frog twitch fibers at 20°C. A and B: recorded action potentials. The fiber in A shows a monotonic decrease in the early afterpotential and that in B shows a secondary hump. C: calculated action potential; the T system has been represented as a passive lumped admittance. [From Adrian et al. 6.] D: calculated action potential; the T system has been represented as a distributed admittance in series with an access resistance, and a regenerative increase in sodium conductance has been assumed to occur in the T system following depolarization. (R. H. Adrian and L. D. Peachey, personal communication.)

From Persson 294
Figure 12. Figure 12.

Calculated action potential in a frog twitch fiber 120 μm in diameter. The potential changes are represented as a surface with coordinates of potential (on the vertical axis in 20‐mV divisions), time (on the right horizontal axis in 1‐ms divisions), and radial distance along the T system (on the left horizontal axis in 20‐μm divisions). Diametrically opposite surfaces of the fiber are at the extreme left and right of the distance axis, and the most axial T tubules 60 μm from each surface are located in the center of the distance axis. The delayed onset of depolarization in the axial tubules relative to the fiber surface is clearly seen, and a few‐millivolt hump in the early afterpotential at the fiber surface coincides with the peak depolarization in the axial T tubules. In this calculation the T system has been represented as a distributed admittance in series with an access resistance, and a regenerative increase in sodium conductance has been assumed to occur in the T system following depolarization.

R. H. Adrian and L. D. Peachey, personal communication
Figure 13. Figure 13.

The dependence of isometric tension on myoplasmic calcium in vertebrate muscle. The smooth curve is the relation between the free calcium concentration and isometric tension of a skinned fiber from Xenopus muscle at a sarcomere length of 2.2 μm 91. The lower scale of total myoplasmic calcium was calculated on the assumption that all the bound myoplasmic calcium was associated with troponin. The data for the dependence of calcium binding on free calcium concentration was that of Bremel & Weber 38 for calcium binding to troponin in reconstituted thin filaments with no myosin present, and the troponin concentration of intact vertebrate muscle was taken as 33 μm 78. Although both the tension measurements and the calcium‐binding study employed a Ca‐EGTA buffer system, the calculated free calcium concentrations were different, since different values were chosen for the apparent Ca‐EGTA binding constant. The values used here are those of Endo 91, and the free calcium concentrations calculated by Bremel & Weber 38 were multiplied by 4 for purposes of comparison [see 78]. Although isometric tension and calcium binding by troponin were determined at slightly different ionic strengths and pH's, no attempt has been made to correct for this. (I am grateful for the assistance of Dr. M. Endo in the preparation of this figure.)
Figure 14. Figure 14.

Calcium‐induced calcium release in skinned frog twitch fibers. A skinned fiber immersed in a nutrient ionic medium was exposed to alterations in calcium and EGTA concentrations at the times indicated by the arrows. A: the fiber was transferred from a solution containing 0.1 mM EGTA and no added calcium to a Ca‐EGTA buffered medium (buffered Ca) with a free calcium concentration of 10−6 M. After 30 s free calcium was removed by transfer to 0.1 mM EGTA, and the EGTA concentration was then reduced to 0.01 mM. Exposure to a free calcium concentration of 10−4 M resulted in a prompt contracture. B: the sequence of solution changes was similar to A, but the contracture was interrupted by 1.0 mM EGTA. C: exposure to 10−4 M free calcium following prolonged immersion in 0.01 mM EGTA resulted in a slow increase in contractile force. The force spike elicited by 10−4 M free calcium when the SR was preloaded in a buffered calcium solution was absent.

From Ford & Podolsky 105. Copyright 1970 by the American Association for the Advancement of Science
Figure 15. Figure 15.

Relation between membrane potential and contractile activation in an isolated frog twitch fiber. Curve 1 (right‐hand ordinate), peak contracture tension elicited by a test solution containing the potassium and chloride concentrations indicated on the abscissa. The estimated membrane potential in each solution is given by the lower scale. Curve 2 (left‐hand ordinate), peak contracture tension elicited by 190 mM K+, 2.5 mM Cl− solution following 1 min recovery in the test solution indicated on the abscissa. Curve 3, same as curve 2, but the ordinate is the area under the tension‐time curve for the same contractures.

From Hodgkin & Horowicz 164
Figure 16. Figure 16.

Voltage‐dependent charge movement in a frog twitch fiber. A: upper trace, membrane potential. The holding potential and the magnitude of the depolarizing step are shown below each voltage record. In b, the holding potential was stepped to −126 mV 100 ms before the start of the 41‐mV depolarizing pulse. Lower trace, membrane current recorded as the potential difference between two intracellular microelectrodes with the 3 micro‐electrode voltage‐clamp technique 6. B: effect of pulse duration on charge movement. Each trace shows the difference between the membrane current elicited by a 47‐mV depolarizing pulse from a holding potential of −80 mV and a pulse of equal magnitude from a holding potential of −127 mV. The difference in currents has been signal‐averaged 4 times. Pulse duration: a, 10 ms; b, 20 ms; c, 40 ms; d, 80 ms.

From Schneider & Chandler 316
Figure 17. Figure 17.

Intracellularly recorded action potentials from (A) sheep Purkinje tissue and (B) dog ventricular myocardium. Vertical calibration, 50 mV. Horizontal calibration: A, 500 ms; B, 200 ms.

From Weidmann 353
Figure 18. Figure 18.

Membrane currents in a voltage‐clamped cat ventricular trabecula. Upper trace, clamping current. Middle trace, membrane potential recorded by a test electrode. Lower trace, membrane potential recorded by the voltage‐controlling electrode. The test electrode and the voltage‐controlling electrode were separated by 0.36 mm along the 0.54‐mm clamped segment. The upper trace has been shifted to the right to prevent superimposition of the early transient response. A‐D: preparation in 3.6 mM Ca2+. Increasing depolarizations from a holding potential of −58 mV. E‐H: preparation in 1.8 mM Ca2+. Increasing depolarizations from a holding potential of −56 mV. The fast inward sodium current is seen as a downward spike and a corresponding voltage spike is recorded by the test electrode; the potential at the test electrode is maintained at a steady value after the initial sodium current has subsided. A secondary inward current with a much slower time course than the sodium spike is seen when the magnitude of the depolarizing step is increased; the amplitude of this slow inward current is greater in the 3.6 mM Ca2+ solution.

From New & Trautwein 263


Figure 1.

Sarcomere pattern in striated muscle. An electron micrograph of a longitudinal section through 2 myofibrils of a frog skeletal muscle is shown above, and the overlap of thick and thin filaments that gives rise to the pattern of bands within the sarcomere is illustrated schematically below. The 2 myofibrils are separated by elements of the internal membrane system. The I band is light because it consists only of thin filaments. The A band is dark where it consists of overlapping thick and thin filaments and lighter in the H zone where it consists solely of thick filaments. The M line is caused by a bulge in the center of each thick filament and the pseudo H zone by a central region of the thick filament that lacks cross bridges.

From Huxley 187. Copyright © 1965 by Scientific American, Inc. All rights reserved


Figure 2.

Schematic reconstruction of a small portion of a frog twitch muscle fiber. The longitudinal axis of the fiber runs from left to right. The contractile filaments are grouped into roughly cylindrical myofibrils about 1 μm in diameter, and each myofibril is enveloped by the transverse tubular system (T system) and the sarcoplasmic reticulum (SR). The close association among the T tubule and 2 terminal cisternae of the SR to form a triad is seen in section in the lower portion of the figure. The elliptical T tubule is about 250 × 800 A in diameter.

From Peachey 287


Figure 3.

Schematic representation of the organization of the SR in a frog heart fiber. A portion of the cell membrane is shown together with 2 myofibrils and their associated SR tubules. A large proportion of the tubules partially surrounds the myofibrils at Z‐line level; connected with these are others oriented in a roughly longitudinal direction. At the cell periphery branches of the SR tubules terminate, usually at I‐band level, in disklike structures that form junctional contacts with the surface membrane of the cell.

From Page & Niedergerke 286


Figure 4.

Inward rectification in frog skeletal muscle. The relation between membrane potential and membrane current is shown for a fiber that was studied successively in sulfate solutions containing 50, 100, and 50 mM K+. The membrane current is in arbitrary units; outward current is taken as positive.

From Adrian 4


Figure 5.

Asymmetry in the membrane potential response of single muscle fibers produced by sudden changes in extracellular potassium in chloride‐free sulfate solution. A: normal fiber. B: glycerol‐treated fiber. Each fiber had been equilibrated in 40 mM K+; solution changes, to 165 mM K+ and back to 40 mM K+, are indicated by the small downward deflections in the lower traces.

From Nakajima et al. 252


Figure 6.

An equivalent circuit containing 2 time‐constants that represents the frequency‐dependent impedance of a frog muscle fiber.Rm and Cm represent the impedance of the surface membrane, and Re and Ce, which provide a pathway for current flow in parallel with the surface membrane, represent the impedance of the T system.

From Falk 97


Figure 7.

Current‐voltage relations in a voltage‐clamped barnacle muscle fiber. (—) Peak early transient current in response to 300‐ms test pulses; (—) steady‐state current; (•) test pulse applied from a holding potential equal to resting potential (−50 mV); (☆) test pulse preceded by a 136‐ms conditioning depolarization to −22 mV; (○–○) membrane current before activation of the early transient current. The point in the current trace at which each measurement was made is shown in the inset.

From Hagiwara et al. 135


Figure 8.

Local activation of a frog twitch fiber. Polarized light compensated so that the A bands appear dark. The fiber is immersed in, and the pipette is also filled with, Ringer's solution. An electric pulse is applied to the pipette making the interior of its tip go roughly 100 mV negative relative to the surrounding fluid for a period of about 0.5 s. In the upper part the pipette is applied to an A band, and there is no response. In the lower part the pipette is applied to an I band, and during the pulse that I band (and only that I band) shortens. Grid spacing, 10 μm.

From Huxley & Taylor 185


Figure 9.

Radial pattern of contractions in TTX‐treated and TTX‐free fibers. The 2 voltage‐clamp microelectrodes can be seen impaling opposite sides of each fiber. Grid spacing, 10 μm. A: fiber in normal Ringer's solution with 50 μg TTX per 100 ml. The resting striation spacing was 2.5 μm. Suprathreshold depolarization produces shortening of the superficial myofibrils without waves to a striation spacing of 1.58–1.76 μm, whereas the axial myofibrils are thrown into waves at striation spacings of 1.65–1.79 μm. White line traces the pattern of the waves. B: no TTX present. Resting striation spacing was 2.5 μm. Suprathreshold depolarization produces shortening of the axial myofibrils without waves to 1.58–1.77 μm, whereas the superficial myofibrils are wavy at striation spacings of 1.90–2.00 μm. White lines trace the pattern of the waves.

From Costantin & Taylor 64


Figure 10.

Late afterpotential following trains of action potentials in a frog twitch fiber. Time course of the membrane potential is displayed at 2 different amplifications and 2 different sweep speeds in the 2 traces of each panel. The gain is 4 times greater for the upper trace, and the time scale of 1 s refers to the upper trace. Action potentials are 10 ms apart. The early afterpotential that follows a single impulse can be seen in the lower right panel.

From Freygang et al. 119


Figure 11.

Action potentials in frog twitch fibers at 20°C. A and B: recorded action potentials. The fiber in A shows a monotonic decrease in the early afterpotential and that in B shows a secondary hump. C: calculated action potential; the T system has been represented as a passive lumped admittance. [From Adrian et al. 6.] D: calculated action potential; the T system has been represented as a distributed admittance in series with an access resistance, and a regenerative increase in sodium conductance has been assumed to occur in the T system following depolarization. (R. H. Adrian and L. D. Peachey, personal communication.)

From Persson 294


Figure 12.

Calculated action potential in a frog twitch fiber 120 μm in diameter. The potential changes are represented as a surface with coordinates of potential (on the vertical axis in 20‐mV divisions), time (on the right horizontal axis in 1‐ms divisions), and radial distance along the T system (on the left horizontal axis in 20‐μm divisions). Diametrically opposite surfaces of the fiber are at the extreme left and right of the distance axis, and the most axial T tubules 60 μm from each surface are located in the center of the distance axis. The delayed onset of depolarization in the axial tubules relative to the fiber surface is clearly seen, and a few‐millivolt hump in the early afterpotential at the fiber surface coincides with the peak depolarization in the axial T tubules. In this calculation the T system has been represented as a distributed admittance in series with an access resistance, and a regenerative increase in sodium conductance has been assumed to occur in the T system following depolarization.

R. H. Adrian and L. D. Peachey, personal communication


Figure 13.

The dependence of isometric tension on myoplasmic calcium in vertebrate muscle. The smooth curve is the relation between the free calcium concentration and isometric tension of a skinned fiber from Xenopus muscle at a sarcomere length of 2.2 μm 91. The lower scale of total myoplasmic calcium was calculated on the assumption that all the bound myoplasmic calcium was associated with troponin. The data for the dependence of calcium binding on free calcium concentration was that of Bremel & Weber 38 for calcium binding to troponin in reconstituted thin filaments with no myosin present, and the troponin concentration of intact vertebrate muscle was taken as 33 μm 78. Although both the tension measurements and the calcium‐binding study employed a Ca‐EGTA buffer system, the calculated free calcium concentrations were different, since different values were chosen for the apparent Ca‐EGTA binding constant. The values used here are those of Endo 91, and the free calcium concentrations calculated by Bremel & Weber 38 were multiplied by 4 for purposes of comparison [see 78]. Although isometric tension and calcium binding by troponin were determined at slightly different ionic strengths and pH's, no attempt has been made to correct for this. (I am grateful for the assistance of Dr. M. Endo in the preparation of this figure.)



Figure 14.

Calcium‐induced calcium release in skinned frog twitch fibers. A skinned fiber immersed in a nutrient ionic medium was exposed to alterations in calcium and EGTA concentrations at the times indicated by the arrows. A: the fiber was transferred from a solution containing 0.1 mM EGTA and no added calcium to a Ca‐EGTA buffered medium (buffered Ca) with a free calcium concentration of 10−6 M. After 30 s free calcium was removed by transfer to 0.1 mM EGTA, and the EGTA concentration was then reduced to 0.01 mM. Exposure to a free calcium concentration of 10−4 M resulted in a prompt contracture. B: the sequence of solution changes was similar to A, but the contracture was interrupted by 1.0 mM EGTA. C: exposure to 10−4 M free calcium following prolonged immersion in 0.01 mM EGTA resulted in a slow increase in contractile force. The force spike elicited by 10−4 M free calcium when the SR was preloaded in a buffered calcium solution was absent.

From Ford & Podolsky 105. Copyright 1970 by the American Association for the Advancement of Science


Figure 15.

Relation between membrane potential and contractile activation in an isolated frog twitch fiber. Curve 1 (right‐hand ordinate), peak contracture tension elicited by a test solution containing the potassium and chloride concentrations indicated on the abscissa. The estimated membrane potential in each solution is given by the lower scale. Curve 2 (left‐hand ordinate), peak contracture tension elicited by 190 mM K+, 2.5 mM Cl− solution following 1 min recovery in the test solution indicated on the abscissa. Curve 3, same as curve 2, but the ordinate is the area under the tension‐time curve for the same contractures.

From Hodgkin & Horowicz 164


Figure 16.

Voltage‐dependent charge movement in a frog twitch fiber. A: upper trace, membrane potential. The holding potential and the magnitude of the depolarizing step are shown below each voltage record. In b, the holding potential was stepped to −126 mV 100 ms before the start of the 41‐mV depolarizing pulse. Lower trace, membrane current recorded as the potential difference between two intracellular microelectrodes with the 3 micro‐electrode voltage‐clamp technique 6. B: effect of pulse duration on charge movement. Each trace shows the difference between the membrane current elicited by a 47‐mV depolarizing pulse from a holding potential of −80 mV and a pulse of equal magnitude from a holding potential of −127 mV. The difference in currents has been signal‐averaged 4 times. Pulse duration: a, 10 ms; b, 20 ms; c, 40 ms; d, 80 ms.

From Schneider & Chandler 316


Figure 17.

Intracellularly recorded action potentials from (A) sheep Purkinje tissue and (B) dog ventricular myocardium. Vertical calibration, 50 mV. Horizontal calibration: A, 500 ms; B, 200 ms.

From Weidmann 353


Figure 18.

Membrane currents in a voltage‐clamped cat ventricular trabecula. Upper trace, clamping current. Middle trace, membrane potential recorded by a test electrode. Lower trace, membrane potential recorded by the voltage‐controlling electrode. The test electrode and the voltage‐controlling electrode were separated by 0.36 mm along the 0.54‐mm clamped segment. The upper trace has been shifted to the right to prevent superimposition of the early transient response. A‐D: preparation in 3.6 mM Ca2+. Increasing depolarizations from a holding potential of −58 mV. E‐H: preparation in 1.8 mM Ca2+. Increasing depolarizations from a holding potential of −56 mV. The fast inward sodium current is seen as a downward spike and a corresponding voltage spike is recorded by the test electrode; the potential at the test electrode is maintained at a steady value after the initial sodium current has subsided. A secondary inward current with a much slower time course than the sodium spike is seen when the magnitude of the depolarizing step is increased; the amplitude of this slow inward current is greater in the 3.6 mM Ca2+ solution.

From New & Trautwein 263
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Article Title: Activation in Striated Muscle
 

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L. L. Costantin. Activation in Striated Muscle. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 215-259. First published in print 1977. doi: 10.1002/cphy.cp010107