Book - Comparative Embryology of the Vertebrates 4-16

The Muscular System

A. Introduction

1. Definition

2. General structure of muscle tissue

a. Skeletal muscle

b. Cardiac muscle

c. Smooth muscle

B. Histogenesis of muscle tissues

1. Skeletal muscle

2. Cardiac muscle

3. Smooth muscle

C. Morphogenesis of the muscular system

1. Musculature associated with the viscera of the body

2. Musculature of the skeleton

a. Development of trunk and tail muscles

1 ) Characteristics of trunk and tail muscles in aquatic and terrestrial vertebrates

a) Natatorial adaptations

b) Terrestrial adaptations

c) Aerial adaptations

2) Development of trunk and tail musculature

a) General features of myotomic differentiation in the trunk

b) Differentiation of the myotomes in fishes and amphibia

c) Differentiation of the truncal myotomes in higher vertebrates and particularly in the human embryo

d) Muscles of the cloacal and perineal area

e) Development of the musculature of the tail region

b. Development of muscles of the head-pharyngeal area

1) Extrinsic muscles of the eye

2) Muscles of the visceral skeleton and post-branchial area

a) Tongue and other hypobranchial musculature

b) Musculature of the mandibular visceral arch

c) Musculature of the hyoid visceral arch

d) Musculature of the first branchial arch

e) Muscles of the succeeding visceral arches

f) Muscles associated with the spinal accessory or eleventh cranial nerve

g) Musculature of the mammalian diaphragm

c. Development of the musculature of the paired appendages

d. Panniculus carnosus

699

700

THE MUSCULAR SYSTEM

A. Introduction

1. Definition

The muscular system produces mobility of the various body parts. As such, it is composed of cells specialized in the execution of that property of living matter which is known as contractility. Since contractility is a generalized property of living matter, it may occur without the actual differentiation of muscular tissue. In the developing heart of the chick, for example, contractures begin to occur as early as 33 to 38 hours of incubation before muscle cells, as such, have differentiated (Patten and Kramer, â€™33).

2. General Structure of Muscle Tissue

Muscle cells are elongated, fibrillated structures, known as muscle fibers. They contain many elongated fibrils, called myofibrils, extending longitudinally along the muscle fiber. The myofibrils may possess a series of cross striations in the form of light and dark transverse bands as in skeletal or striated muscle and cardiac muscle, or the transverse bands may be absent as in smooth muscle (fig. 325 A-C). In smooth muscle, the myofibrils are extremely fine, whereas in striated muscle they are seen readily under the microscope.

a. Skeletal Muscle

In skeletal muscle, the muscle fibers are elongated, cylinder-shaped structures; the ends are rounded; and a row of nuclei extend along the periphery of the muscle fiber or cell, and are more numerous at the ends of the cell than in the central portion. The cell, as a whole, is filled with myofibrils, embedded in a matrix of sarcoplasm. The latter contains fat droplets, glycogen, interstitial granules, amino acids, mitochondria, and Golgi substances. The surrounding cell membrane is a delicate structure and is known as the sarcolemma.

The myofibrils are composed of dark and light transverse bands, a dark band alternating with a light band. The bands are arranged along the myofibrils in such a manner that the dark band of one fibril is at the same level as the dark bands of other fibrils. The light bands are arranged similarly. This arrangement presents the effect shown in figure 325A.

Two types of muscle fibers are found in skeletal muscle. In one type, the red or dark fiber, there is an abundance of sarcoplasm with fewer myofibrils. The myofibrils possess weaker transverse markings or striations. In the second type, the pale or white fiber, there is less of the sarcoplasm present with a larger number of highly differentiated myofibrils, having well-defined transverse striations. This muscle fiber is larger in transverse diameter than the red type. In many animals, such as man, these two sets of fibers are intermingled in the various skeletal muscles, but in some, such as the breast

INTRODUCTION

701

muscles of the common fowl, the white fibers constitute most of the muscle. Also, in the M. quadratus femoris of the cat or the M. semitendinosus of the rabbit, the red fiber predominates. In general, the more continuously active muscles contain the greater number of red fibers, while the less continuously active contain pale fibers. Pale fibers react more quickly and thus contract more readily than the red fibers. However, they are exhausted more rapidly.

Connective tissue, mostly of the white fibrous variety, associates the muscle fibers (cells) into groups called muscles. Muscles, such as the Mm. biceps brachii, biceps femoris, sartorius, rectus abdominis, etc., are a mass of associated muscle fibers, tied together by connective-tissue fibers.

The surrounding connective tissue of a particular muscle is known as the external perimysium (fig. 325D). The external perimysium extends centralwaref into the muscle and separates it into smaller bundles of fibers, or fasciculi. Thus each fasciculus is a group of muscle fibers, surrounded by the internal perimysium. The perimysium around each fasciculus extends into the fasciculus between the muscle cells, where its fibers become associated with the sarcolemma of each muscle fiber (cell).

The connection between the muscle fibers and their tendinous attachment has attracted considerable interest. One view holds that the myofibrils pass directly into the tendinous fibers. An alternative and more popular view maintains, however, that it is the sarcolemma which attaches directly to the tendinous fibers. Hence, the pull of the muscle is transmitted through the sarcolemmas of the various muscle cells to the tendon.

b. Cardiac Muscle

Cardiac muscle is characterized by the presence of alternating dark and light bands as in skeletal muscle. The striations are not as well developed, however, as in skeletal muscle, nor is the sarcolemma around the muscle fibers as thick. Another distinguishing feature of cardiac muscle is the fact that the fibers anastomose and thus form a syncytium, although M. R. Lewis (T9) questions this interpretation. Still another characteristic structure of cardiac muscle is the presence of the intercalated discs (fig. 325C). These discs are heavy transverse bands which extend across the fiber at variable distances from one another. A final feature which distinguishes cardiac muscle is the central location of the nuclei within the anastomosing fibers.

c. Smooth Muscle

Smooth muscle fibers are elongated, spindle-shaped elements which may vary in length from about 0.02 mm. to 0.5 mm. The larger fibers are found in the pregnant uterus. The diameter across the middle of the fiber approximatess 4 to 7 /i. This middle area contains the single nucleus. The fiber

702

THE MUSCULAR SYSTEM

tapers gradually from the middle area and may terminate in a pointed or slightly truncate tip (fig. 325B).

Smooth muscle cells may contain two kinds of fibrils:

(1) fine myofibrils, presumably concerned with contraction phenomena, within the cytoplasm and

(2) myoglial or border fibrils, coarser than the myofibrils, in the peripheral areas of the cell.

The myoglial fibrils are not usually demonstrable in adult tissues.

A connective-tissue mass of fibers between the smooth muscle fibers which binds the fibers into bundles as in skeletal muscle is not readily demonstrated. It may be that a kind of adhesiveness or stickiness (Lewis, W. H., â€™22) associates these muscle fibers into a mass, within which each muscle cell is a distinct entity and not part of a syncytium. However, around the muscle bundles, elastic and white fibers (Chap. 15) seem to hold the muscle tissue in place and some elastic fibers may be present between the cells, especially in blood vessels.

B. Histogenesis of Muscle Tissues 1. Skeletal Muscle

The primitive embryonic cell which gives origin to the later muscle cells is called a myoblast. The myoblasts which give origin to skeletal muscle fibers are derived from two sources:

(1) mesenchyme and

(2) myotomes.

(See Chap. 11 for origin of mesenchyme and myotomes; also consult fig. 252.)

In striated-muscle-fiber formation, the myoblasts begin to elongate and eventually produce cylinder-like structures. As the cell continues to elongate, the nuclei increase in number, and, hence, the myoblast becomes converted into a multinuclear affair in which the nuclei at first lie centrally along the axis of the cell. Later, the myofibrils increase, and the nuclei move peripherally.

As the myofibrils grow older, dark and light areas appear along the fibrils. These dark and light bands are shown in figure 325E. Observe that the light band is bisected by the slender membrane, known as Krauseâ€™s membrane, shown in the figure as the dark line, Z., and the dark band is bisected by Hensenâ€™s membrane.

2. Cardiac Muscle

The musculature of the vertebrate heart takes its origin from the two mesial walls of hypomeric fnesoderm (i.e., the splanchnic layers of mesoderm) which come to surround the endocardial primordia or primitive blood capillaries

HISTOGENESIS OF MUSCLE TISSUES 703

coursing anteriad below the foregut (Chap. 17). These two enveloping layers of mesoderm give origin to the epicardium and myocardium of the heart, and in consequence they are referred to as the epimyocardial rudiment. From the surfaces of the two layers of hypomeric mesoderm which face the primitive blood capillaries, mesenchymal cells are given off. These mesenchymal cells constitute the myocardial primordium. The outer wall of each hypomeric layer of mesoderm, however, retains its epithelial character and eventually gives origin to the epicardium or coelomic covering of the heart. The mesenchymal cells which form the myocardial primordium surround the two endocardial rudiments (blood capillaries) and later form an aggregate of coalesced cells, i.e., a syncytium. The future heart musculature arises from this syncytium.

As the mass of the myocardial syncytium increases in size, the nuclei become irregularly scattered, and myofibrils make their appearance. The number of myofibrils rapidly increases, and dark bands of anisotropic substance (i.e., substance which is doubly refractive under polarized light) alternate with lighter bands of isotropic substance. Z lines soon appear which bisect the lighter segment of the myofibrils.

The myofibrils increase, and the myocardial syncytium gradually becomes drawn out into elongated strands of cytoplasm which appear to anastomose (fig. 325C). The nuclei are scattered within these strands. As the myofibrils

704

THE MUSCULAR SYSTEM

DORSAL SEPTUM ARCUALE NEURAL TUBE VERTEBRAL BODY LATERAL SEPTUM DORSAL AORTA

mesenchyme gives:

ORIGIN TO SMOOTH MUSCLE TISSUE

VENTRAL SEPTUM

DORSAL RIB

EPAXIAL MUSCULATURE (STRIATED MUSCLE TISSUE)

EPIDERMIS LATERAL SEPTUM HYPAXIAL MUSCULATURE (STRIATED MUSCLE TISSUE)

.yfj INTERDORSAL I

BASIDORSAL I

ARCUALIA

^^^â– interventral [ZZZI Â®AS'VENTRAL J D.

Fig. 326. Arrangement of muscle tissues. (A) Ventricles of alligator heart, ventral aspect, showing spiral arrangement of superficial muscle layers. (Redrawn from Shaver, Anat. Rec., 29.) (B) Arrangement of smooth muscle layers of the stomach. (Redrawn

from Bremer, 1936, Textbook of Histology, Philadelphia, Blakiston, after Spalteholz. ) (C) Transverse section of tail of Squalus acanthias showing arrangement of epaxial and hypaxial muscle groups. (D) Primitive arrangement of myotomes into epaxial and hypaxial groups in relation to the myocommata or myosepta. Observe that the myoseptum attaches to the middle of the vertebra. (Redrawn and modified from Goodrich, Vertebrate Craniata, 1909, New York, Macmillan Co., and Kingsley, Comparative Anatomy of Vertebrates, 1912, Philadelphia, Blakiston.

continue to increase, they become aggregated into groups and are arranged in such a manner that the dark and light bands of adjacent fibrils form regular dark and light bands across the muscular strands. The intercalated discs finally make their appearance here and there across the muscle strands (fig. 325C). In some areas, there are no nuclei within the muscle strand between the intercalated discs.

3. Smooth Muscle

Smooth muscle, cells arise from mesenchyme. In doing so, the mesenchymal cells lose their stellate shapes, elongate, and eventually become spindle shaped. Accompanying these changes, the nuclei experience some extension in the direction of the elongating cells (fig. 325B). Fibrils appear in the cytoplasm, first at the periphery in the form of coarse fibers, to be followed somewhat later by the true myofibrils of finer texture. It is possible that the coarser fibrils, the so-called myoglial fibers, represent bundles of myofibrils. The

MORPHOGENESIS OF MUSCULAR SYSTEM

705

myofibrils in smooth muscle fibers do not assume anisotropic (dark) and isotropic (light) bands or cross striations. Increase in the number of muscle fibers (cells) appears to occur by the mitotic division of existing fibers and also by the transformation of other mesenchymal cells.

C. Morphogenesis of the Muscular System

1. Musculature Associated with the Viscera of the Body

The musculature associated with the viscera of the body is of the smooth type with the exception of cardiac muscle and anterior part of the esophagus. Smooth and cardiac musculature are under involuntary control. The smooth muscle tissue of the digestive tract is derived from mesenchyme, which arises from the inner or splanchnic layers of the hypomeres, while that of the urinary and genital systems takes its origin from nephrotomic mesoderm and contributions from the splanchnic layers of the two hypomeres (fig. 311 A, B). The smooth muscle tissue associated with many of the blood vessels of the body arises from mesenchymal sources in the immediate area of the blood vessels.

The arrangement of muscle tissue in various parts of the digestive tract, blood vessels, and urinary and reproductive ducts is generally in the form of circular and longitudinal layers (fig. 325B). On the other hand, the myocardium or muscle tissue of the heart is an association of layers or sheets which tend to be wound in complex spirals. Particularly is this true of the ventricular portion of the heart (fig. 326A). Also, in the stomach, the arrangement of the muscle layers is complex, being composed of an outer longitudinal layer, a middle circular layer, and an inner, somewhat spirally arranged, oblique layer (fig. 326B), The general pattern of arrangement of smooth and cardiac muscle tissues shows much similarity throughout the vertebrate group.

2. Musculature of the Skeleton

The skeletal musculature is striated and under voluntary control. It is that musculature which moves various parts of the endoskeleton and integumental structures, enabling the animal to adapt itself to surrounding environmental conditions. The development of skeletal musculature will be described under the following headings:

(a) development of trunk and tail muscles,

(b) development of muscles of the head-pharyngeal area,

(c) development of the musculature of the paired appendages, and

(d) development of the panniculus carnosus in Mammalia.

a. Development of Trunk and Tail Muscles

1) Characteristics of Trunk and Tail Muscles in Aquatic and Terrestrial Vertebrates. In endeavoring to understand the development of the trunk and

706

THE MUSCULAR SYSTEM

tail musculature in the vertebrate group as a whole, it is important that one consider the environment in which the various species live, for the trunk and tail musculature is adapted to the general functions of moving the animal in its particular habitat. We may recognize three main environmental adaptations :

(1) natatorial,

(2) terrestrial, and

(3) aerial.

a) Natatorial Adaptations. Animals, adapted to swimming, possess a different arrangement of the musculature of the trunk and tail regions than do terrestrial and aerial forms. A transverse section through the tail of the dogfish, Squalus acanthias, demonstrates that the musculature is arranged around the vertebrae in a definite pattern. A horizontal skeletogenous septum extends outward from either side, dividing the muscles on each side of the vertebra into epaxial and hypaxial groups, and dorsal and ventral septa are present in the middorsal and midventral areas (fig. 326C).

Viewed laterally, the muscles are divided by transverse membranes, the muscle septa, myosepta, or myocommata (figs. 326D; 327A). The position of the myocomma corresponds to the intermyotomic (intersegmented) area observed in Chapter 15. Each myocomma is attached to the vertebral body (really several vertebral bodies). The myotomes (fig. 326D) lie in the segmented position between the myocommata and are attached to the latter. In the tail, both these groups of muscles are attached to the myocommata and the vertebrae, but, farther forward in the trunk, it is the epaxial group which is associated directly with the myocommata and the vertebrae, the hypaxial group being less direct in its contact with the vertebral column. (See fig. 31 IB.) In figure 327B, the myotomes and myosepta (myocommata) have a Z-shaped appearance because of a secondary modification during development.

It is evident, therefore, that in the shark, the skeletal muscles of the trunk and tail exist in the form of segments, each segment being divided into an upper epaxial and lower hypaxial component. This arrangement of the muscles and the attachment of the fibers to the myosepta, and thus through the myoseptum to the vertebra, produces a mechanism exceedingly well adapted to the side-to-side movement of the vertebral column so necessary during natation. The conditions present in the sharks are comparable to those of other fishes, and, in all, the epaxial musculature is exceedingly well developed.

b) Terrestrial Adaptations. In the land-frequenting vertebrates, there is less development of and dependence upon the tail region and the dorsal or epaxial musculature for locomotive purposes. In consequence, the epaxial musculature is segregated on either side of the vertebrae in a dorsal position, while the hypaxial musculature and its derivatives in the bilateral appendages are expanded ventrally. The suppression of epaxial muscle development is carried to an extreme form in the aerial adaptations of the bird. In non

MORPHOGENESIS OF MUSCULAR SYSTEM

707

aquatic forms the tail musculature is greatly reduced, and in some forms is almost non-existent.

A consideration of the effect that locomotive habits have upon musculature development may be shown by a brief comparison of the musculature in a water-living amphibian, such as Necturus, and in a land-going adventurer, such as the frog. In Necturus, the dorsal (epaxial) musculature, the primitive M. dorsalis trunci, is more like that of the fish, with the muscle fibers attached to the myocommata (fig. 327C), although, contrary to the piscine condition, the muscle fibers close to the vertebrae are attached directly to the vertebrae, where they form short bundles. In the frog, the attachment of the epaxial musculature to the vertebrae is more extensive. Bundles of muscle fibers, the Mm. intertransversarii, pass between the vertebral transverse processes, while Mm. intemeurales connect the transverse processes and spinous processes, respectively, of the vertebrae. A separate muscle, the M. longissimus dorsi, extending from the head to the urostyle, separates from the above-mentioned dorsal muscles (fig. 327D). Although a slight suggestion of myocommata may be present, there is little functional relationship of the myocommata to the vertebrae. Laterally, Mm. coccygeo-sacralis and coccygeo-iliacus also are present as differentiations of the dorsal musculature (fig. 327D). Therefore, a definite formation of special and individual muscles occurs in the dorsal or epaxial musculature of the frog, whereas in Necturus, the dorsal musculature tends to resemble the segmental myotomic condition of the fish. It is to be observed that the dorsal musculature of the frog is adapted to a land-going existence, while the dorsal musculature of Necturus is suited to swimming movements.

A further land adaptation is shown in many salamanders, such as the various species of Desmognathus, where the dorsal trunk musculature differentiates in the neck region into several muscles which insert upon the skull. The latter muscles permit lateral movements of the head.

Turning to the hypaxial musculature, we find that this musculature in Necturus also approaches the condition in fishes. Let us examine this musculature in more detail. In the midventral abdominal area, the fibers assume a primitive, strictly segmental, antero-posterior direction. These muscle bundles form the M. rectus abdominis. Along the lateral side of the body wall, the myosepta (myocommata) are retained between the segmented muscles. However, two layers of muscle fibers are present, an outer thick M. obliquus externus, whose fibers run postero-ventrally, and an inner thin layer, the M. obliquus internus, with fibers coursing antero-ventrally. Turning now to the frog, we find that a segmented rectus abdominis (M. rectus abdominis) is present. In each lateral body wall, an outer external oblique muscle (M. obliquus externus superficialis) runs postero-ventrally, while an internal transverse muscle (M. transversus) courses antero-ventrally (fig. 327D). In Necturus and the frog, therefore, the primitive myotomic condition of the

708

THE MUSCULAR SYSTEM

hypaxial musculature of the shark is disrupted, and the myotomes tend to split into layers or sheets of muscles. This splitting is slight in Necturus and marked in the frog. Also, in the frog, the myocommata are displaced as a part of the muscular-skeletal mechanism, with the exception of the rectus abdominis muscle whose segmentation possibly is a secondary development.

In mammals (fig. 327E), the epaxial musculature is differentiated into a complex of muscles, extending from the sacral area anteriorly into the cervical region and connecting the various vertebrae with each other and the vertebral column with the ribs. The epaxial musculature in the trunk area of the bird is much less developed than it is in the mammal. The hypaxial musculature in both bird and mammal becomes separated into distinct layers, sueh as the external, internal oblique, and transversus muscles. External and internal intercostal muscles are present between the ribs. In the midventral area, the rectus abdominis muscle tends to retain its primitive segmentation.

It is noteworthy to observe that the external and internal intercostal muscles in the mammal appear much the same as the lateral body muscles in Necturus, particularly if we keep in mind the fact that ribs grow out into the myoseptal (myocommal) area (fig. 326D). The external intercostal muscles run posteroventrally, While the internal intercostals pass antero-ventrally from one rib to the next (fig. 327E). The intercostal musculature of the mammal thus retains the primitive, segmented condition.

c) Aerial Adaptations. The musculature of the bird is a highly differentiated organization of structures in which the primitive myotomic plan is greatly distorted. The epaxial musculature is reduced greatly over the trunk region, although well developed in the cervical area. Hypaxial musculature is present in the form of external and internal oblique, and transverse muscle layers. Very short rectus abdominis muscles arc to be found. Aside from the intrinsic muscles of the limbs, a large percentage of the volume of the hypaxial

Fig. 327. Development of branchial and somitic muscles in various vertebrates. (A) Basic areas of the embryo from which skeletal muscle develops. The skeletal muscles of the limb buds are portrayed as masses of mesenchyme represented in this figure as stippled areas in the two limb buds. The origin of this mesenchyme varies in different vertebrates (see text). (B) Skeletal muscular development in the shark. The muscle tissue derived from the hyoid visceral arch is shown in black with white lines. Muscle tissue derivatives from the mandibular visceral arch are shown anterior to the black-white line areas of the hyoid musculature. (C) Same for Necturus maculosus. (D) Same for the frog. (E) Epaxial muscles and intercostal part of hypaxial muscles of cat. External intercostals mostly removed. The â€œmasseter muscle,â€ a derivative of the mandibular visceral arch tissue of the embryo, also is shown. (F/) Superficial facial and platysma muscle distribution in the cat. These muscles are derivatives of the hyoid visceral and mesenchyme. (E") External pterygoid muscle in the cat, another derivative of the branchial arch mesenchyme. (F) Anterior muscles of- the goose. The muscles derived from the primitive hyoid visceral arch are shown in black with white lines. (Adapted from Huber, 1930. Quart. Rev. Biol., vol. 5, and from Furbringer, 1888, Morphologie und Systematik der Vogel, van Holkema, Amsterdam.) (F') The temporal and masseter muscles in the common fowl. These muscles are derived from the mandibular visceral arch.

Fig. 327 . (See facing page for legend.)

709

710

THE MUSCULAR SYSTEM

musculature of the bird is contained within the pectoral muscles (fig. 327F). As such the pectoral musculature represents an extreme adaptation to the flying habit. A somewhat similar adaptation is found among mammals, in the bat group, Myotomic metamerism is much less evident in the bird than in any other group of vertebrates, and the only remains of it appear in the intercostal muscles and some of the deeper muscles of the cervical area.

2) Development of Trunk and Tail Musculature: a) General Features OF Myotomic Differentiation in the Trunk. The muscles of the trunk are derived from the primitive myotomes. As described previously, Chapters 11, 12, and 15, the primitive body segment or somite differentiates into the

MANDIBULAR PROCESS MAXILLARY PROCESS

ATM CERVICAL MYOTOME

ARM MUSCULATURE

ARM SKELETON

ST THORACIC MYOTOME

MESENCHYMAL

PRIMOROlUM OF PECTORAL MUSCLES

VENTRAL (HYPAXIAU REG OF 7TH MYOTOME PORSAL lEPAXIAL) REGION OP TTH MYOTOME

I8T LUMBAR MYOTOME SPINAL GANGLION

41/2 WEEKS

Fig. 328. Muscle development in the human embryo. (A and B redrawn from Bardeen and Lewis, 1901, Am. J. Anat., 1.) (A) Early division of truncal myotomes into dorsal

^enaxial) and ventral (hypaxial) regions.

MORPHOGENESIS OF MUSCULAR SYSTEM

711

HYOID SWELLINGS OF EXTERNAL EAR

TRAPEZIUS

DORSAL MUSCULATURE OF SCAPULA

DELTOID (CUT

LEVATOR SCAPULAE AND

SERRATUS anterior LATISSIMUS OORSI

and

TERES MAJOR

EXTERNAL OBLIQUE

SACROSPINALIS (EPAXIAL MUSCULATUfl

RECTUS FEMORIS

FIRST LUMBAR NERVE

GLUTEAL MUSCLES

Fig. 328 â€” (Continued) Muscle development in the human embryo. (A and B redrawn from Bardeen and Lewis, 1901, Am. J. Anat., 1.) (B) Differentiation of myotomal

derivatives in 11-mm. embryo. Observe that the dorsal division of the spinal nerves is distributed to the epaxial musculature, while the lateral division of the ventral rami passes to the intercostal areas.

sclerotome, myotome, and â€™dermatome (fig. 252). After the sclerotome has departed toward the median plane, the myotome and dermatome reconstruct the dermo-myotome which has a myocoelic cavity within (fig. 311 A). The inner layer or myotome gives origin to the muscle fibers of the later myotome. The fate of the dermatome or cutis plate is not definite in all vertebrates. In lower vertebrates it is probable that most of the dermatome gives origin to dermal mesenchyme (Chap. 12). However, in mammals, according to Bardeen (â€™00) in his studies relative to the pig and human, the dermatome or cutis plate gives origin to muscle cells. On the other hand, Williams (â€™10) does

712

THE MUSCULAR SYSTEM

not tolerate this view, but believes, in the chick at least, that the dermatome gives origin to dermal mesenchyme.

The primitive position of the myotome is lateral to the nerve cord and notochord. As development progresses, the individual myotomes grow ventrally toward the midventral line (fig. 327A). As this downgrowth progresses, each myotome becomes separated into dorsal (epaxial) and ventral (hypaxial) segments (fig. 328A). As indicated above and in figure 326D, the ribs grow

MANDIBULAR SWELLING OF EXTERNAL EAR

HYOID SWELLING OF EXTERNAL EAR

EXTERNAL AUDITORY MEATUS

DELTOID

TRAPEZIUS

TERES MINOR

BRACHIALIS

TERES MAJOR

TRICEPS

SERRATUS ANTERIOR

LATISSIMUS DORSI

EXTERNAL OBLIQUE

RECTUS ABDOMINIS sacrospinalis

BENEATH

LUMBO - DORSAL FASCIA' SARTORIUS

QUADRICEPS FEMORISTENSOR FASCIAE LATA GLUTEUS MEDIUS BICEPS FEMORIS GLUTEUS MAXIMUS

UMBILICAL

ARTERIES

â€¢UMBILICAL VEIN TIBIALIS ANTICUS

EXTENSOR H ALLUCIS LONGUS

EXTENSOR DIGITORUM LONGUS

Fig. 329. Later development of nuisculature in human embryo. (A after Bardeen and Lewis, 1901, Am. J. Anat., 1.) (A) Limb and superficial trunk musculature of 20-mm.

human embryo.

PECTORALIS

TRICEPS STERNUM BRACHIALIS

SPINAL GANGLION NEURAL PROCESS TRAPEZIUS SUPRASPINATUS DELTOID CLAVICLE MAJOR

BRACHIORAOIALIS AND EXTENSOR CARPI RADIALIS SUPINATOR

EXTENSOR POLLICIS BREVIS

EXTENSOR POLLICIS LONGUS

EXTENSOR INOICIS

EXTENSOR CARR ULNARIS

SCAPULA

TERES MAJOR SERRATUS ANTERIOR

URETHRAL ORIFICE

BULBOCAVERNOSyS

ISCHIOCAVERNOSUS

SPHINCTER ANI

GLUTEUS MAXIMUS

Fig. 329 â€” (Continued) Later development of musculature in human embryo. (B after Lewis, 1902, Am. J. Anat., 1.) (B) Developing forelimb musculature of human embryo

(lateral aspect of limb). (C) Differentiation of cloacal musculature in human embryo.

713

714

THE MUSCULAR SYSTEM

out in the area occupied by the myocommata or connective tissue partitions between the myotomes, and thus ribs and myocommata are correlated intimately with myotomic differentiations in all lower vertebrates. However, in reptiles, birds, and mammals, the outgrowing ribs travel downward within the connective tissue between the myotomes, but the development of the mycommata are suppressed.

b) Differentiation of the Myotomes in Fishes and Amphibia. In the fishes, as the ventral myotomic progression occurs, the differentiating muscle fibers become united anteriorly and posteriorly to the myocommata. In Necturus and in amphibian larvae, in general, this relationship also is established, but, in addition, the myotomes become separated into sheets or layers. In the frog during metamorphosis, this splitting of myotomes and the segregation of separate layers and bundles of distinct muscles is carried further. Also in the frog, a marked migration of separate bundles of muscle fibers occurs, while the fusion of parts of separate myotomes is indicated in the development of the M. longissimus dorsi which superficially appears to be segmented (fig. 327D). There is a pronounced tendency, therefore, in the development of the frog musculature for the primitive myotomic plan to be distorted and myotomes fuse, split, degenerate or migrate to serve the required functional purpose of the various muscles.

c) Differentiation of the Truncal Myotomes in Higher VerteBRATA AND PARTICULARLY IN THE HuMAN Embryo. The principles of myotomic modification by fusion, splitting into separate components, migration of parts of myotomes away from the primitive position, and degeneration of myotomic structure as exemplified in the developing musculature of the frog, are utilized to great advantage in reptiles, birds and mammals. The end to be served in all instances is the adaptation of a particular muscle or muscles to a definite function.

In the development of the adult form of the musculature in the human embryo, the basic division of the primitive myotomes into dorsal (epaxial) and ventral (hypaxial) regions occurs (fig. 328A). The dorsal region of the myotomes is located alongside the developing vertebrae, dorsal to the transverse processes. The ventral portions of the myotomes pass ventrally external to and between the ribs, enclosing the developing viscera.

In a slightly older embryo, the dorsal or epaxial musculature begins to lose its primitive segmentation, and the myotomes fuse into an elongated myotomic column, extending caudally from the occipital area (fig. 328B). The deeper portions of the myotomes, associated with the developing vertebrae, appear to retain their original segmentation, and the Mm. levatores costarum, interspinales, intertransversarii, and rotatores persist as segmental derivatives of the myotomes. The outer layer of the dorsal or epaxial musculature splits lengthwise into an outer muscle group, the dorsally placed Mm. longissimus dorsi and spinalis dorsi, and a latero- ventral Mm. iliocostalis group (fig.

MORPHOGENESIS OF MUSCULAR SYSTEM

715

328B). (See Lewis, W. H., â€™10.) Between the above two major groups of muscles derived from the epaxial muscle column are other epaxial derivatives such as the semispinalis and multifidus muscles.

The ventral or hypaxial portions of the myotomes overlying the developing ribs fuse into a continuous mass, while the medial portions of the myotomes lying between the ribs give origin to the Mm. intercostales interni and externi. The ventral ends of the fused myotomes on either side of the midventral line split off longitudinally to form the M. rectus abdominis which becomes an elongated sheet, extending from the anterior pectoral area caudal to the differentiating pelvic girdle. The tendency toward segmentation of the two rectus abdominis muscles probably represents a secondary process in man. Tangential splitting of the fused thoracic and abdominal myotomes and migration of the fibers give origin to the Mm. obliquus abdominis externus, obliquus abdominis internus, transversus abdominis, serratus posterior superior, and serratus posterior inferior.

The deep or subvertebral muscles below the vertebral column in the dorsal area are derived from two sources. The Mm. longus colli and longus capitis arise from the migration of myotomic tissue to the ventral vertebral surfaces in the neck region, whereas the Mm. iliopsoas appear to be derived from the musculature of the hind limb (Lewis, W. H., â€™10).

d) Muscles of the Cloacal ai^d Perineal Area. The muscle tissue of the cloaca forms a circle of constricting muscular bands which surround the cloacal opening. These muscular bands are derived from myotomic tissue of the posterior truncal region.

In the higher mammals, the primitive cloacal opening becomes divided during development into anterior urogenital and posterior anal openings, and the cloacal musculature is divided into the musculature associated with the urethra, external genital structures, and the anal sphincter (fig. 329C).

e) Development of the Musculature of the Tail Region. The musculature of the tail arises from the tail-bud mesoderm of the early embryo. This mesenchyme condenses to form myotomic concentrations which later divide into epaxial and hypaxial segments as in the truncal region of the body. These myotomic segments are well developed in all fishes and in the adults of amphibia other than the Anura. In fishes the enlarged condition of the epaxial and hypaxial muscles of the tail region coincides with the elongation of neural spines and hemal processes of the tail vertebrae where they serve the function of moving the caudal fin from side to side. Three main types of caudal fin skeletal arrangement in fishes (see fig. 331B-D) act as the framework for the fin which serves the relatively enormous propulsive force generated by the tail musculature.

In Necturus, in Cryptobranchus, and in other water-dwelling amphibians, and also in crocodilians, whales, etc., the tail musculature is developed to serve the natatorial function which requires a lateral movement of the tail.

716

THE MUSCULAR SYSTEM

On the other hand, the prehensile or grasping movement of the tail of the opossum, or the tails of western-hemisphere monkeys necessitates an extreme adaptation on the part of individual muscle bundles and their attachment to the caudal vertebrae. Similar specializations are found in the writhing tail of the cat group. The wagging movement of the tail of the dog or the swishing motion of the tails of cows, horses and other mammals is the result of the activities of the Mm. abductor caudae internus and abductor caudae externus which appear to be derivatives of the hind-limb musculature.

b. Development of Muscles of the Head-pharyngeal Area

1) Extrinsic Muscles of the Eye. The extrinsic muscles of the eyeball are one of the most constant features of vertebrate morphology. Six muscles for each eye are found in all gnathostomes, innervated by three cranial nerves as follows:

(1) M. rectus superior â€” cranial nerve III,

(2) M. rectus internus or anterius â€” cranial nerve 111,

(3) M. rectus inferior â€” cranial nerve III,

(4) M. rectus externus (posterius or lateralis) â€” cranial nerve VI,

(5) M. obliquus superior â€” cranial nerve IV, and

(6) M. obliquus inferior â€” cranial nerve III.

To these muscles may be added the Mm. retractor oculi of many mammals and the Mm. quadratus and pyramidalis of birds.

In the shark group, the muscles of the eye arise from three pre-otic somites or head cavities, namely, the pre-mandibuiar, mandibular and hyoid somites (figs. 253, 327A). The pre-mandibular somite, innervated by the oculomotorius or third cranial nerve, gives origin to all of the rectus muscles with the exception of the Mm. rectus externus. The Mm. obUquus inferior also arises from the pre-mandibular somite. From the mandibular somite, innervated by the trochlearis or fourth cranial nerve, arises the Mm. obliquus superior, while the hyoid somite gives origin to the Mm. rectus externus (Balfour, 1878; Platt, 1891; Neal, T8). A derivation of eye muscles from three pre-otic somites or mesodermal condensations has been described in the gymnophionan amphibia by Marcus (â€™09), in the turtle by Johnson (M3), in the chick by Adelmann (â€™26, â€™27), and in the marsupial mammal, Trichosurus, by Fraser (â€™15). For extensive references regarding the eye-forming somites or mesodermal condensations, see Adelmann (â€™26, and â€™27).

Various disagreements, concerning the presence or absence of the various head somites and the origin of the eye muscles therefrom, are to be found in the literature. Regardless of this lack of uniformity of agreement, it is highly probable that the premuscle masses of tissue which give origin to the eye muscles in the gnathostomous vertebrates, in general, adhere closely to

MORPHOGENESIS OF MUSCULAR SYSTEM

717

the pattern of the eye-muscle development from three pre-otic pairs of somites as manifested in the shark embryo.

2) Muscles of the Visceral Skeleton and Post-branchial area: a) Tongue AND Other Hypobranchial Musculature. As indicated in figures 253 and 3 27 A, a variable number of post-otic or met-otic somites are concerned with the composition of the head of the gnathostomous vertebrate. In the dogfish, Squalus acanthias, about six pairs of post-otic somites contribute to the structure of the head ( De Beer, â€™22). For most vertebrates, about three pairs of post-otic somites, a conservative estimate, appear to enter into the headâ€™s composition. The hypobranchial musculature in the elasmobranch embryo arises as myotomal buds from the myotomes of posterior head area. These muscle buds migrate ventrad from these myotomes to the hypobranchial region as indicated in figure 253. Associated with this migration of myotomal material is the migration and distribution of the hypoglossal nerve, compounded from the ventral roots of post-otic spinal nerves to this area (fig. 253). In the human, W. H. Lewis (â€™10) favors the view that the tongue musculature arises in situ from the hypobranchial mesenchyme, but Kingsbury (â€™15) suggests the post-otic origin of the tongue musculature for all vertebrates. Regardless of its origin, the tongue musculature is innervated by ventral nerve roots of post-otic segments in higher vertebrates, i.e., the hypoglossal or twelfth cranial nerve. The tongue musculature becomes associated with the basihyal portion of the hyoid arch, which acts as its support. In mammals, the sternohyoid, sternothyroid, and omohyoid muscles are innervated also by the hypoglossal or twelfth cranial nerve. These muscles probably arise from the post-otic myotomes in a manner similar to the tongue musculature.

b) Musculature of the Mandibular Visceral Arch. The mesoderm, associated with this arch, gives origin to the muscles of mastication, and as a result these muscles are innervated by special visceral motor fibers located in the trigeminal or fifth cranial nerve. In the shark, the muscles arising from the mandibular visceral arch tissue are the adductor mandibulae and the first ventral constrictor muscles (fig. 327B); in the frog, the temporal, masseter, pterygoid, and mylohyoid muscles; in the chick, the pterygotemporal, temporal, and digastric muscles; and, in mammals, the temporal, masseter, pterygoid, anterior portion of the digastric, mylohoid, tensor tympani, and tensor veli palatini muscles (fig. 327D, E', E", F, F').

c) Musculature of the Hyoid Visceral Arch. The musculature, which develops from mesenchyme associated with the embryonic hyoid arch, becomes distributed as indicated in figures 327 and 330. It is to be observed that, in the adult shark (fig. 327B), this musculature functions in relation to the hyoid arch. In the adult frog (fig. 327D), it is represented by deep facial musculature or the depressor mandibulae and subhyoideus muscles. In the adult goose (fig. 327F), it is present as the M. sphincter colli, which

718

THE MUSCULAR SYSTEM

represents superficial facial musculature, and the M. depressor mandibulae or deep facial musculature. In mammals (figs. 327E'; 330A-D), the muscles derived from the hyoid arch is distributed over the cervico-facial area as many separate muscles. The musculature derived from the hyoid arch is innervated by the seventh or facial cranial nerve. Reference may be made to the extensive review of the literature by Huber (â€™30, a and b), relative to the facial musculature in vertebrates.

d) Musculature of the First Branchial Arch. The musculature of the first branchial arch is innervated by the glossopharyngeal or ninth cranial nerve. In the shark, the muscle tissue arising from the first branchial arch becomes the constrictor musculature of this arch, but, in the mammal, it gives origin to the stylopharyngeus muscle and to the constrictors of the pharynx.

e) Muscles of the Succeeding Visceral Arches. In the shark, these muscles contribute to the constrictor muscles of the gill arches and are under the domain of the vagus or tenth cranial nerve. In the mammal, this muscle tissue becomes associated with the larynx and with the constrictors of the

pharynx.

f) Muscles Associated with the Spinal Accessory or Eleventh Cranial Nerve. The sternocleidomastoid and trapezius musculature in the human, according to W. H. Lewis (TO), arises from a premuscle mass associated at the caudal end of the pharyngeal area below the post-otic myotomes (fig. 336A). With the musculature arising from this premuscle mass, the spinal accessory or eleventh cranial nerve becomes associated. The trapezius musculature migrates extensively over the scapular area (fig. 329A).

g) Musculature of the Mammalian Diaphragm. The striated musculature of the mammalian diaphragm appears to arise from the ventral portions of the myotomes in the midcervical area. In the human, this diaphragmatic musculature is innervated by the ventral roots of cervical nerves IV and V, while, in the cat, cervical nerves V and VI are involved. These ventral rami give origin to the phrenic nerve, which later migrates posteriad with the diaphragmatic musculature together with the developing diaphragm during the division of the coelomic cavities (Chap. 20).

c. Development of the Musculature of the Paired Appendages

Two main theories have arisen relative to the origin of the paired appendages. One is the gill-arch theory of Gegenbauer (1876) and the fin-fold or lateral-fold theory of Balfour ( 1881 ). According to the theory of Gegenbauer, the limb girdles are modified gill arches, and the limb tissue itself represents a modification of the gill septa and supporting gill rays. The pelvic limbs were produced, according to this theory, by a backward migration of the gill arch involved. The lateral-fold theory, on the other hand, postulated that the paired limbs were derived from longitudinal fin folds. The endoskeleton within the

MORPHOGENESIS OF MUSCULAR SYSTEM

719

NUCHAL PORTION OF PLATYSMA AND POSTAURICUUO-OCCIPITAL MUSCLE GROUP

M.CAPUT ZY60MATICUS M. ZYGOMATICUS

M. TRIANGULARIS M. PLATYSMA

Fig. 330. Facial and cervical muscles in mammals derived from the mesoderm of the hyoid arch. (Redrawn from Huber, 1930, Quart. Rev. Biol., 5.) (A) Opossum (Didel phys). (B) Cat (Felis). (C) New-born baby (white) human. (D) Adult (white) human.

fold arose as a support for the fold in a manner similar to the median fins. The latter theory has the greatest number of adherents today.

The early development of the rudiments of the paired appendages and the properties of the limb field are discussed in Chapter 10, page 508. Relative to the developing limb, the exact origin of the cells which go to make up its intrinsic musculature has been the object of much study. In the elasmobranch and teleost fishes, muscle buds from the myotomes in the vicinity of the developing fin fold unquestionably contribute dorsal and ventral premuscle masses of cells to the limb, which give origin respectively to

1 ) the dorsal, elevator and extensor muscles, and

2) the ventral depressor and adductor muscles of the fin.

720

THE MUSCULAR SYSTEM

In tetrapod vertebrates, however, the exact origin of the cells which enter into the formation of the limbâ€™s intrinsic musculature is open to question. In the amphibia, including Vrodela and Anura, Field (1894) described myotomic processes which contribute to the musculature of the anterior limbs. Byrnes (1898), working experimentally with the same group, and W. H. Lewis (â€™10b) deny this conclusion and affirm the somatopleural or in situ

Fig. 331. (A) Innervation of premuscie masses in head and pharyngeal areas, and of myotomes in the cervical and caudal head regions of 7-mm. human embryos. Four post-otic (occipital) myotomes and the premuscle mass of the trapezius and sternomastoid muscles are shown just back of the tenth cranial nerve. The first cervical myotome and spinal nerve are shown just posterior to the fourth occipital myotome. (Redrawn from W. H. Lewis, 1910, chap. 12 in Manual of Human Embryology, vol. 1, by F. Keibel and F. P. Mall, Philadelphia, Lippincott.) (B, C, D) Types of caudal fins in fishes.

MORPHOGENESIS OF MUSCULAR SYSTEM

721

origin of the limb musculature and connective tissues. Similar affirmations and denials are found in the literature, relative to origin of the intrinsic limb muscles in higher vertebrates, including man. For example, Ingalls (â€™07) described myotomic cell migrations into the developing human limb, whereas W. H. Lewis (â€™10a) was not able to subscribe to this view.

Although actual muscle tissue from the myotomes to the limb buds cannot be traced in all cases, the fact remains that the nerve supply to a myotome or to a particular group of muscle-forming cells appears to be a constant feature. For example, the facial musculature, which is derived from the hyoid arch mesenchyme of the embryo as set forth above, retains its innervation by the facial or seventh cranial nerve, even though the muscle migrates far forward from its original site of development. The innervation of the trapezius muscle by the spinal accessory nerve is another example of this same fidelity of the nerve supply to the original site of the origin of the muscle-forming cells. Mall (1898, p. 348) describes this relationship between the nerves and myotomes as follows: â€œAs the segmental nerves appear, each is immediately connected with its corresponding myotome, and all of the muscles arising from a myotome are always innervated by branches of the nerve which originally belonged to it.â€ (See fig. 331 A.)

The development of the musculature of the tetrapod limb involves two main premuscle masses of tissue:

( 1 ) An intrinsic mass of muscle-forming mesenchyme within the developing limb which condenses to form separate muscle-forming associations of cells around the developing skeleton of the limb. Each of these cellular associations then proceeds to differentiate into a particular muscle or closely integrated group of muscles (figs. 328B; 329 A and B). That is, the intrinsic mass of muscle-forming tissue gives origin to the intrinsic musculature of the limb.

(2) An extrinsic mass of premuscle tissue which ultimately gives origin to the musculature which attaches the limb and its girdle to the axial skeleton. This premusclc tissue arises from two sources:

(a) Premuscle tissue from the limb bud which migrates from the limb bud proximally toward the axial skeleton. In the forelimb, the pectoral, latissimus dorsi, and teres major muscles develop from this mass of tissue, while in the hind-limb the caudo-femoralis, iliopsoas, piriformis, and certain of the gluteal muscles appear to arise from muscle -forming tissue which extends axially to unite the limb with the axial skeleton.

(b) Premuscle tissue which arises outside the limb bud mesenchyme. The muscles which arise from this tissue serve to attach the limb girdle to the axial skeleton. From premuscle tissue of this type arise the Mm. trapezius, sternocleidomastoideus, rhomboidei, levator scapulae, serratus anterior, and omohyoideus.

722

THE MUSCULAR SYSTEM

d. Fannie ulus Carnosus

There are two groups of skeletal â€œskin muscles,â€ that is, muscles under voluntary control which move the skin and skin structures. One group is the mimetic or facial musculature, described on page 717 and originating from the primitive hyoid mesoderm; the other is the panniculus carnosus, found only in the Mammalia and derived embryologically from the tissue which forms the pectoral musculature. The facial musculature is innervated by cranial nerve VII or the facial nerve, while the panniculus carnosus receives its innervation from the anterior thoracic nerves (fig. 327E').

The panniculus carnosus is highly developed in the guinea pig and porcupine and, although less developed in the rabbit, cat, dog, and horse, it forms a prominent muscular layer. The fibers may be divided into two groups:

(a) fibers which arise and insert in the superficial fascia of the skin and

(b) fibers that arise in the superficial fascia of the back and thigh and converge toward the greater tuberosity of the humerus, where they insert.

For extensive references and descriptions, see Langworthy ('24 and '25).

Bibliography

Adelmann, H. B. 1926. The development of the premandibular head cavities and the relations of the anterior end of the notochord in the chick and robin. I. Morphol. 42:371.

. 1927. The development of the eye muscles of the chick. J. Morphol. 44:29.

Balfour, F. M. 1878. A monograph on the development of elasmobranch fishes. Chap. X in The Works of Francis Maitland Balfour. Edited by M. Foster and A. Sedgwick. Vol. 1, 1885. Macmillan and Co., London.

. 1881. On the development of the skeleton of the paired fins of elasmobranchii, considered in relation to its bearings on the nature of the limbs of the Vertebrata. Chap. XX in The Works of Francis Maitland Balfour. Edited by M. Foster and A. Sedgwick. Vol. 1, 1885. Macmillan and Co., London.

Bardeen, C. R. 1900. The development of the musculature of the body wall in the pig. Johns Hopkins Hospital Reports. 9:367.

Byrnes, E. F, 1898. Experimental studies on the development of limb-muscles in Amphibia. J. Morphol. 14:105.

De Beer, G. R. 1922. The segmentation of the head in Squalus acanthius. Quart. J. Micr. Sc. 66:457.

Field, H. H. 1894. Die Vornierenkapsel, ventrale Musculatur und Extremitatenanlagen bei den Amphibien. Anat. Anz. 9:713.

Fraser, E. A. 1915. The head cavities and development of the eye muscles in Trichosurus vulpecula with notes on some other marsupials. Pr6c. Zool. Soc., London, sA. 299.

Gegenbaur, C. 1876. Zur morphologie der Gliedmaassen der Wirbelthiere. Morph. Jahrb. 2:396.

Huber, E. 1930a. Evolution of facial musculature and cutaneous field of Trigeminus. Part I. Quart. Rev. Biol. 5:133.

. 1930b. Evolution of facial musculature and cutaneous field of Trigeminus. Part 1. Quart. Rev. Biol. 5:389.

Ingalls, N. W. 1907. Beschreibung eincs menschlichen Embryos von 4:9mm. Arch. f. mikr. Anat. u. Entwicklngsgesch. 70:506.

Johnson, C. E. 1913. The development of the prootic head somites and eye muscles in Chelydra serpentina. Am. J. Anat. 14:119.

Kingsbury, B. F. 1915. The development of the human pharynx. Part 1. The pharyngeal derivatives. Am. J. Anat. 18:329.

Langworthy, O. R. 1924. The panniculus carnosus in cat and dog and its genetical relationship to the pectoral musculature. J. Mammalogy. 5:49.

. 1925. A morphological study of the panniculus carnosus and its genetical relationship to the pectoral musculature in rodents. Am. J. Anat. 35:283.

Lewis, M. R. 1919. The development of cross-striations in the heart muscle of the chick embryo. Johns Hopkins Hosp. Rep. 30:176.

Lewis, W. H. 1910a. Chap. 12, Development of the Muscular System in Human Embryology. Edited by Keibel and Mall. J. B. Lippincott Co., Philadelphia.

. 1910b. The relation of the myo tomes to the ventrolateral musculature and to the anterior limbs in Amblystoma. Anat. Rec. 4: 183.

. 1922. The adhesive quality of

cells. Anat. Rec. 23:387.

Mall, F. P. 1898. Development of the ventral abdominal walls in man. J. Morphol. 14:347.

Marcus, H. 1909. Beitrage zur Kenntnis der Gymnophionen. III. Zur Entwicklungsgeschichte des Kopfes, I Teil. Morph. Jahrb. 40:105.

Neal, H. V. 1918. The history of the eye muscles. J. Morphol. 30:433.

Patten, B. M. and Kramer, T. C. 1933. The initiation of contraction in the embryonic chick heart. Am. J. Anat. 53:349.

Platt, J. B. 1891, A contribution to the morphology of the vertebrate head, based on a study of Acanthias vulgaris. J. Morphol. 5:79.

Williams, L. W. 1910. The somites of the chick. Am. J. Anat. 11:55.

Cite this page: Hill, M.A. (2024, April 16) Embryology Book - Comparative Embryology of the Vertebrates 4-16. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Book_-_Comparative_Embryology_of_the_Vertebrates_4-16

What Links Here?