Table Of ContentHandbook of Microscopic Anatomy
Continuation of Handbuch der mikroskopischen Anatomie des Menschen
Founded by Wilhelm von Mollendorff
Continued by Wolfgang Bargmann
Edited by A. Oksche and L. Vollrath
Henning Schmalbruch
Skeletal Muscle
With 129 Figures
Springer-Verlag Berlin Heidelberg NewY ork Tokyo
Handbook of Microscopic Anatomy
Volume II/6: Skeletal Muscle
Privatdozent Dr. H. Schmalbruch
K0benhavns Universitet, Panum Instituttet, Neurofysiologisk Institut,
Blegdamsvej 3 C, DK-2200 K0benhavn N
Professor Dr. Dr. h.c. A. Oksche
Institut ffir Anatomie und Zytobiologie der Justus Liebig-Universitiit, Aulweg 123, D-6300 Giessen
Professor Dr. L. Vollrath
Anatomisches Institut der Johannes Gutenberg-Universitiit, SaarstraBe 19-21, D-6500 Mainz
ISBN -13:978-3-642-82553-8 e-ISBN -13:978-3-642-82551-4
DOl: 10.1007/978-3-642-82551-4
Library of Congress Cataloging in Publication Data. Schmalbruch Henning, 1938- Skeletal muscle.
(Handbook of microscopic anatomy; vol. 11/6) Bibliography: p. Includes indexes. 1. Striated
muscle - Anatomy. 2. Histology. I. Title. II. Series. [DNLM: 1. Muscles - anatomy & histology.
2. Muscles - pathology. QS 504 H236 Bd. 2 T. 6] QM571.S36 1985 611'.73 85-12642
ISBN-13:978-3-642-82553-8 (U.S.)
This work is subject to copyright. All rights are reserved, whether the whole or part of the material
is concerned, specifically those of translation, reprinting, reuse of illustrations, broadcasting, repro
duction by photocopying machine or similar means, and storage in data banks. Under § 54 of
the German Copyright Law where copies are made for other than private use a fee is payable
to "Verwertungsgesellschaft Wort", Munich
© by Springer-Verlag Berlin Heidelberg 1985
Softcover reprint of the hardcover 1st edition 1985
The use of registered names, trademarks, etc. in this publication does not imply, even in the absence
of a specific statement, that such names are exempt from the relevant protective laws and regulations
and therefore free for general use.
Product liability: The publisher can give no guarantee for information about drug dosage and applica
tion thereof contained in this book. In every individual case the respective user must check its
accuracy by consulting other pharmaceutical literature.
2122/3130-543210
Preface
This volume is intended to cover research in the field of muscle morphology
since publication of the previous edition by Haggquist in 1956. The development
of new techniques, coupled with an intensified interest in muscle, has resulted
in a vast literature which no single person could review, especially within the
limitations of one volume. When I accepted the flattering offer to write a new
edition, I quickly abandoned any hope of a comprehensive review. Instead,
I tried to consider, within my limits, those lines of research which I believe
to be important for the understanding of mammalian and ultimately human
muscles under normal, experimental, and pathological conditions. It would be
naive to suggest that muscle can be adequately described in purely morphologi
cal aspects; I would characterize the results of my effort as "muscle as seen
with the eyes of a morphologist".
It gives me pleasure to acknowledge the help of several colleagues who
read and commented on drafts of individual chapters: Dr. Brenda Eisenberg,
Chicago; Dr. Else Nygaard, Copenhagen; Dr. Stefano Schiaffino, Padova; Dr.
Michael Sjostrom, Umea; Dr. Lars~Erik Thornell, Umea. None of these individ
uals can be held responsible for any error or obscurity that persists. Indeed,
without their assistance there would have been more. I also thank those col
leagues who allowed me to include their published and unpublished material;
their names, and also those of the publishers who kindly granted copyright
permission, are given in the individual figure captions.
I am indebted to Mrs. E. Fischer and Mrs. M. L0vgren for their patience
in typing the successive versions of the manuscript, Mr. F. Riis for preparing
the original diagrams, and Mr. A. Dj0rup, engineer, for his assistance with
the word processor.
lowe a deep debt of gratitude to Mrs. M. Bjrerg for many years of coopera
tion in the laboratory. Mrs. Bjrerg double-checked all references, and we sincerly
hope that the list of references will still be useful when future achievements
have antiquated this review. I am grateful, too, to the publishers for expert
processing of this monograph.
I gratefully acknowledge the financial support of my work by the Danish
Medical Research Council. '
I want to dedicate this book to the memory of my friend, Gustav G.
Knappeis, Offenbach-Germany 1899 - H0rsholm-Denmark 1981.
K0benhavn HENNING SCHMALBRUCH
Contents
A. General Overview 1
B. Microanatomy of Muscle 5
I. The Array and Length of Skeletal Muscle Fibres 5
II. The Diameter of Skeletal Muscle Fibres 10
III. The Number of Fibres of a Muscle . 12
IV. The Connective Tissue of the Muscle 14
1. Endomysium . . 16
2. Perimysium 20
V. The Vascular Supply 22
VI. Nerve Supply . . . 30
1. Composition of Nerve Branches to Muscles 30
2. The Number of Motor Units and Its Determination 30
3. The Terminal Innervation Ratio 32
VII. Muscle Spindles 33
C. Skeletal Muscle Fibres 35
I. The Contractile Apparatus 35
1. Cross-Striation . . . . 35
2. Myofibrils . . . . . . 37
3. The Arrangement of Myofilaments in Sarcomeres 39
4. The Localization of the Contractile Proteins 50
5. The Cross-Banding Pattern at Different Fibre Lengths 51
6. The Sliding Filament Model 53
7. X-Ray Diffraction of Muscle . . . . . . . . 54
a) Equatorial Reflections ........ 55
b) Meridional and Off-Meridional Reflections 57
8. The Thick Filament ........... 58
a) The Myosin Molecule . . . . . . . . . 58
b) The Packing Pattern of the Myosin Molecules 59
c) The Number of Myosin Molecules and of
Cross-Bridges per Subunit Repeat . . . . . 62
d) C Protein . . . . . . . . . . . . . . . 63
e) The Periodicities of the A Band of Vertebrate
Muscle . . . . . . . . . . . . 65
f) Myosin ATPase and Cytochemistry 66
9. The Thin Filament . . . . . . . 66
a) The Array of Actin Monomers . . 66
VIII Contents
b) The Pitch of the Actin Helix 67
c) Tropomyosin and Troponin 68
d) A Thin-Filament Model . . 69
e) Binding Sites for the Cross-Bridges 69
10. Morphological Changes of the Thick-Filament
Structure During Rigor and Contraction . . . 70
11. Swinging Cross-Bridges . . . . . . . . . . 74
12. The Regulatory Proteins and the Action of ATP
and Ca2+ . . . . . . . . . . 76
13. Alternative Contraction Theories 77
14. The M Line . . . . . . . . . 79
15. The Z Disc ......... 82
16. The Turnover Rates of Myofibrillar Proteins 90
17. Helicoidal Sarcomeres ..... 90
II. Cytoskeletal Elements . . . . . 91
III. Sarcoplasmic Reticulum and T System 95
1. Historical Background . . . 95
2. The Sarcoplasmic Reticulum 97
a) Array ........ 97
b) Morphological Methods for the Study of Ca2+
Movements and Internal Membrane Changes During
Contraction ....... 102
c) Other Ca2+ -Binding Systems ....... 104
d) The SR Membrane ........... 105
e) The Effect of Various Drugs and of Electrical
Stimulation on Ca2+ Release from the SR 107
3. The T System . . . . . . . 108
a) Array ........ 108
b) The T-Tubule Membrane 109
4. Triadic Junctions ..... 110
5. Very Fast Muscles . . . . . 114
6. Quantitative Approaches to the Internal Membrane
Systems ...... 114
IV. Sarcolemma .......... . 116
1. Historical Background . . . . . 116
2. The Non-Membrane Components 116
3. The Plasma Membrane ..... 119
a) Functional Differences Betweeq Junctional and
Extrajunctional Membrane .,. . . . . . . 119
b) The Structure of the Neuromuscular Junction 120
a) The Presynaptic Membrane 124
{3) The Postsynaptic Membrane 127
y) Acetylcholinesterase . . 127
J) Acetylcholine Receptors 129
e) Quantitative Aspects 130
c) The Extrajunctional Plasma Membrane 131
Contents IX
oc) Folds and Caveolae . . 132
13) 10-nm Particles . . . . 135
y) 6-nm Particles in Square Arrays 137
J) The Extrajunctional Plasma Membrane and
the Motor Nerve . . . . . . . . . . . 138
e) Birefringence Changes of the Plasma Membrane
During Excitation . . . 139
d) The Myotendinous Junction 139
V. Metabolic Systems . . . . . . . 142
1. Mitochondria . . . . . . . . 142
a) The Array of Muscle Mitochondria 142
b) Isolated Mitochondria . . . . 146
c) Training and Hypoxia . . . . 146
d) Intramitochondrial Crystalloids 147
2. Glycogen .......... 148
a) The Intracellular Localization 148
b) The f3-Glycogen Granule 150
c) "Glycogen Paracrystals" 151
3. Intracellular Triglycerides 152
VI. Myonuclei ..... 153
VII. The Lysosomal System . . 155
D. Muscle Fibre Types in Mammalian Muscles 159
I. Historical Background .. . . . . . . . . . . . . .. 159
II. Anaerobic and Aerobic Energy Metabolism of Muscle Fibres
as Reflected by Morphology . . . . 160
1. Preferred Pathways of Metabolism . . . . . . 160
2. The Glycogen Depletion Method ...... 161
3. Method-Related Problems of Fibre Type Histo-
chemistry ................ 162
III. Fast and Slow Muscle Fibres and Their Histochemical
Correlates ................. 162
1. Myosin ATPase and Fibre Typing . . . . . . 162
2. Myosin Heterogeneity and Immunofluorescence 166
IV. Fibre Type Classification and the Physiological
Properties of Motor Units . . . . . . . . . . 173
1. First Attempts and Confusing Nomenclat;ures 173
2. Species Differences ........... 174
3. How Many Fibre Types Can Be Distinguished? 177
V. What Determines the Specialization of Muscle Fibres? 179
VI. The Developement of Muscle Fibre Types 181
1. Histochemistry .. . . . . . . . 181
2. Myosin Isoenzymes . . . . . . . 183
VII. Non-Neural Influences on Fibre Types 185
x Contents
VIII. The Fibre Type Composition of Different Muscles in
Different Species . . . . . . . . . 188
IX. Fibre Types and Electron Microscopy 195
E. Slow Muscle Fibres . . . . . 205
I. Amphibia . . . . . . . 205
1. Felderstruktur Fibres 205
2. Histochemistry 206
3. Twitching and Non-Twitching Slow Fibres 206
4. Ultrastructure 207
II. Birds . . . . . . .. 209
III. Mammals . . . . . . 210
1. Extraocular Muscles 210
a) Two Sorts of Slow Fibres 210
b) Histochemistry and Ultrastructure 211
c) The Force Contribution of Slow Fibres 212
2. Inner Ear Muscles 214
3. Cremaster 215
4. Oesophagus 215
IV. Comments 215
F. Non-Skeletal Muscles 217
I. Extraocular Muscles 217
1. Fish . . . 217
2. Reptiles 217
3. Amphibia 218
4. Birds 218
5. Mammals 218
6. Conclusions 220
II. Intrafusal Muscle Fibres 221
1. Reptiles 221
2. Amphibia 222
3. Birds 223
4. Mammals 223
a) Fibre Types 223
b) Efferent Innervation 229
c) Branching Intrafusal Fibres 232
III. Laryngeal Muscles . . . 232
IV. The Oesophageal Muscle 236
V. Inner Ear Muscles . 236
VI. Mandibular Muscles 237
VII. Facial Muscles 238
G. Development, Regeneration, Growth 239
I. An Overview 239
Contents XI
II. Myogenic Cells .... 241
1. The Origin of Myogenic Cells 241
2. Myoblasts . . . . . . . . 242
a) MyoblastsIn Vitro 242
b) Stages of Differentiation 243
c) Transdifferentiation . . 249
d) Myoblasts In Vivo . . . 250
e) The Morphology of Myoblasts in Culture 251
t) Satellite Cells . . . . 251
g) Fusion of Myoblasts . . . . . . 258
III. Myotubes and Muscle Fibres ..... 263
1. Muscle Fibres as Multinucleated Cells 263
2. Myotube Differentiation 264
a) Myofilaments . . . . . . . . . 264
b) Intermediate Filaments . . . . . 266
c) Sarcoplasmic Reticulum and T System 267
d) Innervation . . . . . . . . . . . . 268
()() Acetylcholine Receptors and Acetylcholinesterase 268
fJ) Neuromuscular Contacts 270
y) Polyneural Innervation 272
3. Histogenesis ....... 274
IV. Regeneration ....... 280
1. Epimorphic and Tissue Modes 280
2. Muscle Fibre Necrosis 281
3. Regeneration In Situ . . . 282
4. Autografts . . . . . . . 284
5. Muscle Fibre Regeneration 286
V. Muscle Fibre Growth 297
1. Transverse Growth 297
2. Longitudinal Growth 300
H. Muscle Fibres as Members of Motor Units 304
I. Definition ........... 304
II. The Size of a Motor Unit . . . . . 304
III. The Array of the Muscle Fibres of a Motor Unit 307
IV. How Are Motor Units of Different Types Used? 309
References 312
A.uthor Index 385
Subject Index 429
A. General Overview
Skeletal muscles develop force and cause movement. The parenchymal cells
of the muscle tissue are multinucleated syncytia, the muscle fibres, which may
be more than 10 cm long. Most muscles consist of one set of fibres, i.e. the
fibres do not act in series. Each fibre contains serially arranged sarcomeres
the length of which changes from 1.3 to 3.5 pm during shortening and stretching,
demonstrating the variable length of the muscle fibre.
The contractile properties of the muscle fibres and its function in the body
determine the internal architecture of a muscle. The load and the shortening
velocity are inversely related. The maximum force during isometric contractions
depends on the cross-sectional area, and short muscles develop force with little
energy. Prestretching increases the force of a muscle fibre; maximum force
is produced at the" optimum sarcomere length", which in situ is attained when
the joint is in a midposition such that the sarcomere lengths of the agonist
and antagonist are about the same. If the maximum shortening velocity per
sarcomere at zero load is given, the shortening velocity of the muscle depends
only on the number of sarcomeres in series; hence, long muscles are best suited
for rapid (or long-range) movements.
Parallel-acting muscle fibres or chains of fibres must have the same number
of sarcomeres - otherwise they would shorten at different speeds. The fibres
insert in a staggered fashion; they form a parallelogram together with the tendon
sheets at which they insert. The endplate is close to the middle of a fibre,
and the endplates of a muscle are usually concentrated in narrow endplate
zones. A muscle may have the form of only one parallelogram and be unipen
nate, or of several parallelograms and be multipennate. Correspondingly, it
may have one or several endplate zones. The volume of a shortening muscle
fibre remains constant; the angle of insertion increases during contraction, and
the parallelogram becomes wider to provide space for the thickening of the
musCle fibres. This protects the blood vessels and the intramuscular nerve
branches. Fusiform muscles with converging fibres do not exist; the fibres would
be sheared off from their insertion by the increase in circumference during
shortening.
The coarse collagen bundles of the perimysium are arrayed in a way that
they do not interfere with the displacement of the fascicles of muscle fibres
in relation to each other; the collagen bundles only hold the muscle fibres
together. Each individual muscle fibre is surrounded by a fine network of heli
cally wound collagen fibrils which are part of the sarcolemma. They are slack
at rest length, but become taut and longitudinally oriented when the fibre is
stretched; there is then an increased resistance to stretch. The myofibrils, along
the entire length of the fibre, are mechanically linked across the plasma mem-
