Book - Comparative Embryology of the Vertebrates 4-15

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Nelsen OE. Comparative embryology of the vertebrates (1953) Mcgraw-Hill Book Company, New York.

Comparative Vertebrate Embryology 1953: 1. The Period of Preparation | 2. The Period of Fertilization | 3. The Development of Primitive Embryonic Form | 4. Histogenesis and Morphogenesis of the Organ Systems | 5. The Care of the Developing Embryo | Figures

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Part IV - Histogenesis and Morphogenesis of the Organ Systems

Part IV - Histogenesis and Morphogenesis of the Organ Systems: 12. Structure and Development of the Integumentary System | 13. Structure and Development of the Digestive System | 14. Development of the Respiratory-buoyancy System | 15. The Skeletal System | 16. The Muscular System | 17. The Circulatory System | 18. The Excretory and Reproductive System | 19. The Nervous System | 20. The Development of Coelomic Cavities | 21. The Developing Endocrine Glands and Their Possible Relation to Definitive Body Formation and the Differentiation of Sex

The Skeletal System

A. Introduction

1. Definition

The word skeleton is used commonly to denote the hard, supporting framework of the body, composed of bone and cartilage. In this restricted sense it is employed to refer particularly to the internal or endoskeleton (see p. 668). The word has a broader meaning, however, for the skeletal system includes not only the bony and cartilaginous materials of the deeper-lying, internal skeleton but also the softer, pliable connective tissues as well. Thus, the skeletal tissues in a comprehensive sense may be divided as follows:

1. the soft skeleton, composed of pliable connective tissues which bind together and support the various organs of the body and
2. the hard or firm skeleton, formed of bone, cartilage, and other structures which protect and sustain, and give rigidity to the body as a whole. The exoskeletal structures described in Chapter 12 in reality are a part of the hard, protective skeleton of the vertebrate body.

{Note: Blood and lymph are often classified as a part of the connective tissues. See Maximow and Bloom, ’42, p, 39.)

Fig. 311. (A) Diagram showing basic mesenchymal packing tissue around the various body tubes and notochord. (B) Contribution of embryonic mesenchyme to adult skeletal tissue.

2. Generalized or Basic Embryonic Skeleton; Its Origin and Significance

a. Basic Condition of the Skeletal System

The generalized or basic skeleton of the embryo which has achieved primitive body form is composed of the notochord or primitive skeletal axis, together with the mass of mesenchyme which comes to fill the spaces between the epidermal, neural, enteric, mesodermal, and primitive circulatory tubes. Because of the delicate nature of the mesenchymal cells and the coagulable intercellular substance between them, this primitive skeleton sometimes is referred to as the “ghost skeleton” (fig. 31 1 A).

b. Origin of the Primitive Ghost Skeleton

1) Notochord and Subnotochordal Rod. As observed in Chapters 9 and 10, the notochord becomes segregated as a distinct entity during gastrulation and embryonic body formation. It soon comes to form a rod-like structure, surrounded by a primitive notochordal membrane. The notochordal axis extends from the pituitary body (hypophysis) and diencephalic region of the brain caudally to the end of the tail (fig. 217). In many of the lower vertebrates, a second rod of cells, the hypochord or subnotochordal rod, evaginates and segregates from the roof of the gut in the trunk region of the embryo during tubulation and early body-form development; it comes to lie immediately below the notochord (fig. 228). The subnotochoral rod soon degenerates.

The notochord never extends cranialward beyond the hypophysis and infundibular downpushing from the diencephalon in any of the vertebrates. This meeting place of the hypophysis, notochord, and infundibulum is a constant feature of early vertebrate structure from the cyclostomatous fishes to the mammals. In Amphioxus, however, the notochord projects anteriad beyond the limits of the “brain” (fig. 249D, E).

2) Origin of the Mesenchyme of the Early Embryonic Skeleton, The origin of mesenchyme in the early embryo is set forth in Chapter 1 1 , page 520.

c. Importance of the Mesenchymal Packing Tissue of the Early Embryo

The mass of mesenchymal cells which comes to lie between the embryonic body tubes not only forms the primitive skeletal material of the early embryo but it also serves as a reservoir from which later arise many types of cells and tissues, as indicated in the following diagram: endothelial cells of capillaries and other blood vessels "^lipoblasts â–ºfat cells

chondroblasts (cartilage-forming cells) â–ºchondrocytes

and cartilage

✓fibroblasts ►fibrous connective tissue

^osteoblasts â–ºosteocytes and bony substances, including

Mesenchymal dermal bones and the dermal substances of scales

cells macrophages â–ºphagocytes

^hemocytoblast (free, wandering, mesenchymal cell) erythrocytes Vyrnonocytes

blood platelets 'white blood cells 'myoblasts (for smooth, cardiac.

and skeletal muscle)

In regard to the skeletal system, it is pertinent to point out the fact that wherever mesenchyme exists, the possibility for connective tissue development also exists,

B. Characteristics and Kinds of Connective Tissues

Connective tissues, other than adipose tissue, are characterized by the presence of intercellular substances which become greater in quantity than the cellular units themselves. In consequence, the various types of connective tissue are classified in terms of the intercellular substance present. Excluding the blood, three main categories of connective tissues are found:

( 1 ) connective tissue proper,

(2) cartilage, and

( 3 ) bone.

CHARACTERISTICS OF CONNECTIVE TISSUES

1. Connective Tissue Proper

The connective tissues proper may be divided into

(a) fibrous types and

(b) fatty or adipose tissue.

a. Fibrous Types

1) Reticular Tissue. This type of connective tissue possesses stellate cells, between which are found delicate aggregations of fibrils and a fluid-like, intercellular substance (fig. 3126).

2) White Fibrous Tissue. White fibrous tissue contains bundles or sheets of white, connective-tissue fibers (i.e., collagenous fibers), placed between the cells. Some clastic fibers may be present (fig. 312C, D). Collagenous fibers yield gelatin upon boiling with water and are not digested readily by trypsin (Maximow and Bloom, ’42).

3) Elastic Tissue. Elastic connective tissue is similar to the white fibrous variety but contains a large percentage of elastic tissue fibers which extend under stress but contract again when tension is released (fig. 312E). Elastic fibers are resistant to boiling water and are digested readily by trypsin (Maximow and Bloom, ’42). Elastic tissue may have a yellowish tinge when viewed macroscopically.

Fig. 312. Types of soft connective tissues. (A, D, and E redrawn from Bremer, 1936, Textbook of Histology, Philadelphia, Blakiston; B and C redrawn from Keibel and Mall, 1910, Manual of Human Embryology, vol. I, Philadelphia. Lippincott; F redrawn from Bell, ’09.)

Fig. 313. Types of cartilaginous tissue. (A-C) Development of hyaline cartilage. (D) Destruction of cartilage by perichondrial vascular bud preparatory to ossification. The cartilage spicules may be infiltrated with calcium salt at this period. (Redrawn from Bremer, 1936, Textbook of Histology, Philadelphia, Blakiston.) (E) Fibrocartilage, from area of tendinous union with bone. (F) Elastic cartilage from human, larynx. (Redrawn and modified from Bremer, 1936, Textbook of Histology, Philadelphia, Blakiston.)

b. Adipose Tissue

Adipose tissue contains a fibrous network of white and elastic fibers, between which fat cells develop. Eventually, the fibrous connective tissue is displaced and pushed aside by the fat-containing elements (fig. 312F).

2. Cartilage

Cartilage is a type of connective tissue with a solid intercellular substance. The latter is composed of a fibrous framework filled with an amorphous ground substance. Unlike bone, the intercellular substance may be readily cut with a sharp instrument. Three main types of cartilage are found:

( 1 ) hyaline,

(2) fibrous, and

(3) elastic.

a. Hyaline Cartilage

Hyaline cartilage (fig. 313A-C) is the most widespread variety of cartilage. It is characterized by a solid, amorphous, ground substance, slightly bluish in appearance, easily bent and capable of being cut with a sharp instrument.

The amorphous ground substance or chondrin is reinforced by fibers of the collagenous (white) variety, but the quantity of fiber present is much less than in fibrous or elastic cartilage. The chondrocytes (i.e., the cartilage cells) lie within capsules. Canaliculi apparently do not connect one capsule with another. This type of cartilage forms a considerable part of the temporary axial and appendicular skeleton of the developing organism and remains as the adult axial and appendicular skeleton in cyclostomatous and elasmobranch fishes. In the adults of other vertebrates, it is supplemented to various degrees by bone.

b. Fibrocartilage

Fibrocartilage (fig. 313E) is a transitional form between white fibrous connective tissue and cartilage. It contains bundles of collagenous fibers, placed parallel to each other. Between the fibrous bundles, cartilage capsules are present, containing cartilage cells (chondrocytes). A small amount of amorphous ground substance or chondrin is present, particularly around the cell capsules. Some types of fibrocartilage contain more of the amorphous ground substance than other types. Fibrocartilage is found in the intervertebral discs between the vertebrae, in the area between the two pubic bones in mammals, and in certain ligaments, such as the ligamenlum teres femoris.

c. Elastic Cartilage

Elastic cartilage (fig. 313F) differs from the hyaline variety by the presence of an interstitial substance which contains branching and interlacing fibers of the elastic variety. The elastic fibers penetrate through the amorphous substance in all directions. While hyaline cartilage is bluish in color, the color of elastic cartilage is yellowish. It is found in the external ear of mammals, in the mammalian epiglottis, Eustachian tubes, the tubes of the external auditory meatus, etc.

3. Bone

a. Characteristics of Bone

Bone forms the greater part of the adult skeleton of all vertebrates above the cyclostomatous and elasmobranch fishes. In teleost fishes and in landfrequenting vertebrates, it tends to displace most of the cartilaginous substance of the skeleton. The interstitial substance of bone is composed of a fundamental fibrous material similar to that of connective tissue. These fibers are called osteocollagenous fibers. A small amount of amorphous ground substance also is present. The interstices of this fibrous and amorphous substrate are infiltrated with mineral salts, particularly calcium salts, to form the bony substance. The latter is formed in layers, each layer constituting a lamella. The bone cells or osteocytes are present in small cavities or lacunae between the lamellae. The lacunae are connected with each other by small channels or canaliculi which course through the lamellae. Some of the canaliculi join larger channels within the bony substance which contain blood vessels. Bony substance in the living animal, therefore, is living tissue, constructed of the following features (fig. 314):

1. Bony layers or lamellae are present, composed of a ground substance of fibrous and amorphous materials infiltrated with mineral salts, particularly the salts of calcium (fig. 314A, B);
2. between the bony layers are small cavities or lacunae, each containing a bone cell or osteocyte (fig. 314B);
3. coursing through the lamellae and connecting the various lacunae, are small channels, known as canaliculi, into which extend processes from the osteocytes (fig. 314B); and
4. the canaliculi make contact in certain areas with blood vessels which lie within small canals coursing through the bony substance or in larger spaces, called marrow cavities (fig. 314A, B).

Fig. 314. Types and development of bone. (A) Compact and cancellous (spongy) bone. (B) Diagram showing structure of compact bone. (Redrawn and slightly modified from Maximow and Bloom, 1942, A Textbook of Histology, Philadelphia, Saunders.) (C) Stages in conversion of marrow canal or space of* spongy bone into an Haversian system by deposition of concentric layers of bony lamellae. (D) Haversian systems of compact bone from thin, ground section. (Redrawn and modified from Bremer, 1936, Textbook of Histology, Philadelphia, Blakiston.)

Pio. 3l4~(Co/ifi/i/n'i/) Types and development of bone. (H) Diagram showing invasion of eartilage by perichondrial vascular buds, preparatory to deposition of bony substance on cartilaginous spicules produced by erosion of cartilage (compare with fig. 313, D). (F) The formation of spongy bone within, by deposition of bony substance on cartilaginous spicules. See spicule “A.” Compact bone is deposited on outer surface of cartilaginous replica of future bone by periosteal osteoblasts, forming bony cylinder of compact bone. (Redrawn and modified from Bremer, 1936, Textbook of Histology, Philadelphia, Blakiston.) (G) Formation of membrane bone from jaw of pig embryo. (Redrawn and modified from Bremer, 1936, Textbook of Histology, Philadelphia, Blakiston.) (H ) Bone destruction and resorption. Observe osseous globules within substance of osteoclast. (From Jordan, ’21, Anat. Rec., 20.)

b. Types of Bone

From these fundamental structural features, two types of bone are formed:

1. spongy and
2. compact.

The difference between these two types of bone rests upon the proportion of bony substance to blood-vessel area or marrow cavity present, and is not due to a difference in the character of the bony substance itself.

c. Characteristics of Spongy Bone

Spongy bone differs from compact bone in that large marrow cavities or spaces are present between an irregular framework of compact bone. The bony substance present is in the form of a meshwork of irregular columns or trabeculae between the marrow-filled spaces (fig. 314A).

d. Compact Bone

Compact bone (fig. 314A, B, D) lacks the widespread, marrow-filled cavities of the spongy variety, the marrow spaces being reduced to a minimum. This is accomplished by the utilization of a structural unit known as the Haversian system, named after Clopton Havers, an English anatomist who discovered the system during the latter part of the seventeenth century while investigating the blood supply of bone. The bony walls of the shafts of long bones are composed largely of many Haversian systems, associated side by side as shown in figure 314D. Irregular layers (lamellae) lie between the various systems.

The Haversian system is composed of a very narrow canal or lumen, the Haversian canal, around which are placed concentrically arranged bony plates (lamellae) with their associated lacunae, osteocytcs, and canaliculi (fig. 314B-D). Blood vessels from the marrow cavity within the bone or from the surface of the bone via Volkmann’s canals (fig. 314D) pass into the Haversian canals, thus supplying nourishment and other life-maintaining features to the canaliculi and through the latter to the osteocytes. Compact bone thus restricts the marrow cavity to a central area, and the Haversian and Volkmann canals convey the blood supply into the compact bony substance which surrounds the central marrow cavity. In general, the Haversian systems are formed parallel with the long axis of the bone. Circumferential lamellae surround the external surface of the bone around the Haversian systems. Inner circumferential lamellae also are present lining the marrow cavities of long bones.

C. Development of Skeletal Tissues

1. Formation of the Connective Tissue Proper

a. Formation of Fibrous Connective Tissues

In the early embryo, following the ghost-skeleton stage, two types of connective tissues are found:

1. Mucoid or loose connective tissue is located in Wharton’s jelly in the umbilical cord of mammals and in other parts of the embryo. This embryonic type of connective tissue is characterized by the presence of large mesenchymal cells whose processes contact the processes of other surrounding mesenchymal cells (fig. 312A). Within the meshwork formed by these cells and their processes, mucus or a jelly-like substance is present. Very delicate fibrils may lie within this jelly.
2. A second type of early embryonic connective tissue is reticular tissue. It contains stellate mesenchymal cells whose processes contact each other (fig. 312B). Very delicate bundles of fibrils may be present which are closely associated with the cells.

The foregoing, connective-tissue conditions of the early embryo eventually are replaced by the mature forms of connective tissue. In this process the reticular type of connective tissue appears to form an initial or primary stage of connective-tissue development. For example, in the development of white fibrous tissue, a delicate network of fine fibrils appears within the ectoplasmic ground substance between the primitive mesenchymal cells, thus forming a kind of reticular tissue (fig. 312A, B). With the appearance of fibrils between the mesenchymal cells, the latter may be regarded as fibroblasts. Following this reticular stage, the ectoplasmic ground substance becomes more fibrillated and parallel bundles of white fibers arise, probably by the direct chemical transformation of the earlier fibrils into white or collagenous fibers (fig. 312C). (See Bardeen, ’10, p. 300.) It is probable that the elastic connective tissue with its elastic fibers arise in a similar manner, with the exception that elastic fibers are formed instead of collagenous fibers.

The matter of fiber formation within connective tissues has been the subject of much controversy. The older view of Flemming (Mall, ’02, p. 329) maintains that the fibers arise within the peripheral area of the cytoplasm of the cell from whence they are thrown off into the intercellular space where they continue to grow. However, most observers now agree that the fibrils arise from an intercellular substance, i.e., from the substance lying between the fibroblasts, but the manner by which this intercellular substance itself arises is questionable. Some observers, such as Mall (’02) and Jordan (’39), set forth the interpretation that the intercellular substance is derived from a syncytial ectoplasm which becomes separated from the early mesenchymal cells. Baitsell (’21) and Maximow (’29), however, consider the intercellular substance to be a secretion product of the mesenchymal cells which have become fibroblasts. The observations of Stearns (’40) on living material in a transparent chamber of the rabbit’s ear suggest that the ground substance is exuded by the surface of the fibroblasts and that the fibers then develop within this exudate.

b. Formation of Adipose or Fatty Connective Tissue

Adipose tissue is fibrous connective tissue which contains certain specialized cells of mesenchymal origin, the lipoblasts. The latter have the ability to produce lipoidal substances and to store these substances within the confines of their own boundaries. Adipose or fatty tissue arises in fibrous connective tissues in various parts of the body in proximity to blood capillaries.

Lipogenesis or the formation of the fatty substance is an unsolved problem. Two main types of fat are formed, white and brown. The process of lipogenesis in white fat, according to Schreiner (’15) who studied the process in detail in the hagfish embryo, Myxine glutinosa, consists at first in liberation of small buds from the nucleolus within the nucleus. These buds pass through the nuclear membrane into the cytoplasm as granules or chromidia. In the cytoplasm these granules appear as mitochondria. The latter increase in number by division. The secondary granules then separate and each gives origin to a liposome which liquefies and expands into a small fat globule. Regardless of the exact method by which the small fat globules arise, when once formed, the small globules coalesce to form the large fat globule, typical of white fat, which ultimately pushes the nucleus and cytoplasm of the lipoblast to the periphery (fig. 312F). (Sec Bell, ’09.) Lipoblasts in the mature condition are fat cells or lipocytes.

The above type of fat-cell formation occurs in the subcutaneous areas of the embryo. In the human embryo it begins at about the fourth month. However, aside from the common type or white-fat formation, another kind of fat-cell development occurs in certain restricted areas of the body in the so called brown fat tissue found in certain adipose glands. It is referred to as brown fat because a brownish pigment may be present in certain mammals. During brown-fat formation, mesenchymal cells become ovoid in shape and develop a highly granular cytoplasm. These granules give origin to small fat globules which remain distinct for a time and do not readily fuse to form the large fat globule, characteristic of white fat. However, they ultimately may coalesce and become indistinguishable from the ordinary lipocyte found in white fat. In man, this type of fat disappears shortly after birth; in the cat, it is present until maturity when it transforms into the ordinary type or white fat; and in the rat, it persists throughout life (Sheldon, ’24). In the woodchuck, this type of fat forms the hibernating gland (Rasmussen, ’23). In mice and other rodents, the presence of a small amount of brownish pigment is evident in this type of fat. In the young monkey, hibernating-gland tissue is found in the cervical, axillary, and thoracic areas (Sheldon, ’24).

2. Development of Cartilage

The formation of cartilage is an interesting process. During the initial stage of cartilage development, mesenchymal cells withdraw their processes, assume a rounded appearance, and become closely aggregated. This condition is known as the pre-cartilage stage (fig. 313A). Gradually the pre-cartilage condition becomes transformed into cartilage by the appearance of the intercellular substance, characteristic of cartilage between the cells (fig. 313B, C). As in the case of the connective tissues described on page 664, two schools of thought explain the appearance of this intercellular substance:

(a) as a modification of the ectoplasm which separates from the chondroblasts and

(b) as a secretion of these cells.

In hyaline cartilage, the homogeneous, amorphous, ground substance is predominant, together with a small number of fibrils; in bbrocartilage, a large number of white, connective-tissue fibers and a smaller amount of the amorphous substance is deposited; and in elastic cartilage, elastic, connectivetissue fibers are formed in considerable numbers. The mesenchyme, immediately surrounding the mass of cartilage, forms the specialized tissue, known as the perichondrium. The perichondrial layer, as the name implies, is the tissue immediately surrounding the cartilage. It connects the cartilage with the surrounding connective tissue and mesenchyme. The inner cells of the perichondrium transform into chondroblasts and deposit cartilage; in this manner the cartilage mass increases in size by addition from without. The latter form of growth is known as peripheral growth. On the other hand, an increase within the mass of cartilage already formed is the result of interstitial growth. Interstitial growth is effected by an increase in the number of cells within the cartilage and by a deposition of intercellular substance between the cells. The increase in the intercellular substance separates the chondroblasts from each other, and the mass of cartilage expands as a whole. These two types of growth are important processes involved in the increase in size of many body structures. Cartilage formation in the human embryo begins during the fifth and sixth weeks.

3. Development of Bone

Bone develops as the result of the calcification of previously established fibrous or cartilaginous connective tissues. The transformation of fibrous connective tissue into bone is called membranous or intramembranous bone formation, and the process which transforms cartilage into bone constitutes endochondral or intracartilaginous bone development. Membranous bone formation occurs in the superficial areas of the body, particularly in or near the dermal area of the skin whereas cartilaginous bone formation is found more deeply within the substance of the body and its appendages.

a. Membranous Bone Formation

Membranous bone formation occurs as follows (fig. 314G): Thin spicules or bars of a compact intercellular substance, known as ossein, gradually come to surround collagenous (osteogenic) fibers which lie between fibroblast cells. Later, these spicules of ossein become calcified by the action of specialized cells, called osteoblasts, which surround the osseinated fibrils. Osteoblasts may represent transformed fibroblasts or, more directly, transformed mesenchymal cells. With the deposition of the bone salts, the tissue is converted from ossein into bone. Thus, spicules of ossein and connective tissue fibers serve as the basis for bone deposition and become converted into bony spicules. These spicules are converted next into bony columns (trabeculae) by the formation of layers (lamellae) of compact bone around the original bony spicule. Such bony columns or trabeculae are characteristic of spongy bone (fig. 314A). Some of the bone-forming cells become enclosed within the lacunar spaces in the bone during the above process and are left behind as bone cells or osteocytes (fig. 314A). The osteocytes within their respective lacunae tend to be located between the layers of bony material (fig. 314A-D).

After the primary trabeculae of spongy bone are formed, the surrounding mesenchyme, which encloses the site of bone formation, becomes converted into a membranous structure, known as the periosteum. The cells of the inner layer of periosteum are transformed into osteoblasts and begin to deposit successive layers of compact bone around the initial framework of spongy bone (peripheral growth). The latter activity results in an increase in diameter of the bony area.

The first bone thus formed occurs in a restricted area. As the bone grows, the previously formed bone is torn down and resorbed, while new compact bone is built up around the area occupied by the spongy bone. Either by the formation of new cellular entities or by the fusion of osteoblasts, multinucleated giant cells appear which aid in the dissolution of the previously formed bone. These multinucleate cells are known as osteoclasts (fig. 314H). The marrow-filled spaces between the trabeculae of spongy bone contain blood spaces (sinusoids), developing red blood cells, looser connective tissues, and fat cells (fig. 314H). When the trabeculae of spongy bone are resorbed, the marrow-filled area increases in size.

b. Endochondral and Perichondrial (Periosteal) Bone Formation

While membranous bone development utilizes collagenous fibrils and ossein as a foundation upon which the osteoblasts deposit bone salts, endochondral that is, intracartilaginous bone development employs small spicules or larger masses of cartilage as a basis for calcification. The small columns or spicules of cartilage are produced as a result of erosion and removal of cartilage. This erosion of cartilage is produced by perichondrial cells and vascular tissue which invade the cartilaginous substance from the perichondrium.

1) Endochondral Bone Formation.

Endochondral bone formation occurs as follows:

(a) The initial step in erosion of cartilage is the migration within the cartilage, in a manner not understood, of the scattered cartilage cells. This migration brings about the arrangement of the cartilage cells and their capsules into elongated rows (fig. 314F). Some deposition of calcium within the cartilaginous matrix occurs at this time.

(b) As this realignment of the cartilage cells is effected, vascular buds from the inner layer of the perichondrium invade the cartilage, eroding the cartilaginous substance and forming primary marrow cavities (figs. 31 3D; 314E, F). Large multinucleate cells or chondroclasts make their appearance at this time and aid the process of dissolution of cartilage.

(c) Following this procedure, osteoblasts arise within the peripheral areas of each vascular bud and begin to deposit bone matrix upon the small spicules of calcified cartilage which remain. (See spicule “a,” fig. 314F.) The continual deposition of bone salts around these spicules converts the greatly eroded cartilaginous mass into spongy or cancellous bone (fig. 314F).

2) Perichondrial (Periosteal) Bone Formation. As cancellous bone is formed within the cartilaginous mass, the surrounding perichondrium of the original cartilage now becomes the periosteum, and the cells of the inner layer of the periosteum deposit circumferential layers of compact bone (perichondrial or periosteal bone formation) around the periphery of the cancellous bone (fig. 314F). The latter action forms a cylinder of compact bone around the spongy variety and around the cartilage which is being displaced (fig. 314F). The primary marrow spaces, established by the original invasion of the perichondrial vascular buds, merge to form the secondary marrow areas of the developing bone. This merging process is effected by the dissolution of previously formed bony spicules or trabeculae.

c. Conversion of Cancellous Bone into Compact Bone

Spongy or cancellous bone is converted into compact bone by the deposition of layers of compact bone between the trabeculae or columns of spongy bone, thus obliterating the marrow cavities around the trabeculae of the cancellous bone and converting the intervening areas into Haversian systems (fig. 314C, D).

D. Development (Morphogenesis) of the Endoskeleton

1. Definitions

For pedagogical purposes, the hard, skeletal tissues may be divided into the external skeleton or exoskeleton and the internal skeleton or endoskeleton. The exoskeleton comprises all the hard, protective structures which are derived from the mesenchyme of the dermis and from the epithelium of the epidermis, described in Chapter 12. The exoskeleton as a whole will not be described further.

Excluding the cxoskeleton and the softer, connective-tissue portion of the skeletal tissues, we shall proceed with a description of the morphogenesis of the main skeletal support of the vertebrate body, the endoskeleton. The endoskeleton is composed of the axial skeleton and the appendicular skeleton. The axial skeleton is composed of the skeleton of the head, the skeleton of the trunk, and the skeleton of the tail. The skeleton of the appendages is made up of the pectoral and pelvic girdles and the bony supports for the appendages.

2. Morphogenesis of the Axial Skeleton

a. General Features of the Skeleton of the Head

The cranium or skeleton of the head comprises:

1. the protective parts for the special sense organs and the brain, and
2. the skeleton of the oral area and anterior end of the digestive tract.

That portion of the cranium which protects the brain and its associated, special sense organs may be called the skull, cranium proper, or neurocranium (fig. 3 1 5D) , whereas that which surrounds the anterior portion of the digestive tract and pharyngeal area is known as the visceral skeleton or splanchnocranium (fig. 315D).

Fig. 315. Developmental stages of the chondrocranium in the dogfish, Squalus acanthias. (A and B redrawn from El-Toubi, ’49, Jour. Morph., 84.) (A) Early de velopmental stage, 37-mm. embryo, lateral view. (B) Intermediate stage, 45-mm. embryo, lateral view. (C) Branchiostcgal (gill support) rays attached to ceratobranchial segment of gill arch. (D) Adult stage of chondrocranium (ncurocranium plus splanchnocranium), lateral view.

1) Neurocranium or Cranium Proper.

The ncurocranium is present in three main forms in the vertebrate group:

(1) a complete cartilaginous cranium without dermal reinforcing bones, as in cyclostomatous and elasmobranch fishes (fig. 315D),

(2) an inner cartilaginous cranium, associated with an outer or surrounding layer of bony plates, as in Amia (fig. 316C, D), the adult skull of Necturus and the frog being similar but slightly more ossified (fig. 317B, C), and

(3) an almost entirely ossified cranium, in teleosts, reptiles, birds, and mammals (figs. 318C; 319C, D, E).

Various degrees of intermediate conditions exist between the above groupings.

2) Visceral Skeleton or Splanchnocranium. The splanchnocranium or visceral skeleton consists of a number of cartilaginous or bony arches which tend to enclose the anterior portion of the digestive tube (fig. 315D). They are present in pairs, one arch on one side, the other arch on the other side. The first two pairs are related to the skull in gnathostomes. The succeeding pairs of visceral arches arc associated with the branchial or gill apparatus in fishes and in certain amphibia, such as Necturus.

3) Development of the Skull or Neurocranium. The neurocranium of all vertebrates from the fishes to the mammals possesses a beginning cranial condition in which dense mesenchyme, the so-called desmocranium, comes to surround the brain and its appendages. The membranous cranium is more pronounced in the basal areas of the brain. This pre-cartilage stage is followed by formation of cartilage which results in the development of a chondric neurocranium. A complete cartilaginous neurocranium is not formed in all vertebrate groups, although the ventro-lateral areas of all vertebrate skulls are laid down in cartilage. This basic, chondrocranial condition exists as the first step in skull formation, and it consists of three main regions, composed of cartilaginous rudiments (figs. 316A, 320):

( 1 ) The basal plate area is composed of a pair of parachordal cartilages on either side of the anterior extremity of the notochord, together with the otic capsules, surrounding the otic (ear) vesicles.

(2) A trabecular or pre-chordal plate area lies anterior to the notochord. This area begins at the infundibular-hypophyseal fenestra and extends forward below the primitive forebrain. Two elongated cartilages, the trabecula cranii (fig. 320A) or a single elongated cartilage (fig. 320B), the central stem or trabecular plate, develop in the basal area of this region. With the trabecular area are associated the sphenolateral, orbital or orbitosphenoidal cartilages and the optic capsules. The latter are placed in a position lateral to the orbitosphenoidal cartilages.

(3) A nasal capsular or ethmoidal plate area, associated with the developing olfactory vesicles, later arises in the anterior portion of the trabecular region (figs. 316A, 319A).

This fundamental cartilaginous condition of the vertebrate skull or neurocranium is followed by later conditions which proceed in three ways: (a) In the elasmobranch fishes, an almost complete roof of cartilage is developed, and the various cartilaginous elements fuse to form the cartilaginous neurocranium (fig. 315). This neurocranium enlarges but never becomes ossified, (b) In the ganoid fish, Amia, the frog, Rana, the mud puppy, Necturus, etc., the basic, ventrolaterally established, cartilaginous neurocranium is converted into a more or less complete chondrocranium by the formation of a roof and the complete fusion of the various eartilaginous elements (figs. 316A-C; 317A, B). In these forms, the cartilaginous cranium becomes ossified in certain restricted areas. In addition to this cartilaginous neurocranium, superficial, membrane bones (dermal bones) are added to the partially ossified chondrocranium. These membrane bones come to overlie and unite with the partly ossified cartilaginous skull (figs. 316D; 317C). (Consult also Table 1.) The adult skull or neurocranium in these forms thus is composed of a chondrocranial portion and an osteocranial part, the osteocranial part arising from cartilaginous and membranous sources, (c) In reptiles, birds, mammals, and in many teleost fishes, the basic ventro-lateral regions of the cartilaginous neurocranium only are formed (figs. 318A, B; 319A, B). This basic chondrocranium undergoes considerable ossification, forming cartilage bones, which replaces the cartilage of the chondrocranium. These cartilage bones are supplemented by superficially developed membrane bones which become closely associated with the cartilage bones. The adult skulls of these vertebrates are highly ossified structures, composed of cartilage and membrane bones. (See Tables 2 and 3.) A few cartilaginous areas persist in the adult skull, more in teleost fishes than in the reptiles, birds, and mammals (Kingsley, ’25 and De Beer, ’37).

4) Vicissitudes of the Splanchnocranium. The early visceral skeleton, established in the embryo, experiences many modifications in its development in the different vertebrate groups.

In the elasmobranch fishes, the first visceral (mandibular) arch on either side gives origin to an upper jaw element, composed of the palatoquadrate (pterygoquadrate) cartilage, and a lower jaw element or Meckel's cartilage

Fig. 316. Developmental stages of neurocranium of the bowfin, Amia calva. (A and B redrawn from De Beer, ’37, after Pehrson; C and D from Allis, 1897, J. Morph., 12.) (A) Ventral view of 9.5-mm. stage. (B) Dorsal view of 19.5-mm. stage. (C) Cartilaginous neurocranium of adult stage. (D) Dermal (membrane) bones overlying neurocranium of adult stage. Cartilage == coarse stipple; bone = fine stipple.

Fig. 317. Developmental stages of neurocranium in the frog. (A and B redrawn from De Beer, ’37, after Pusey; C, redrawn and modified from Marshall, 1893, Vertebrate Embryology, New York, Putnam’s Sons.) (A) Intermediate condition between larval and adult form. (B) Adult form of cartilaginous cranium, present after metamorphosis. (C) Adult neurocranium composed of membrane and cartilage bones associated with basic cartilaginous neurocranium (see Table 1). Cartilage == coarse stipple; bone = fine stipple.

Beer, ’37, from De Beer and Barrington.) (A) Dorsal view of 8 Vi -day stage of Anas (duck). (B) Lateral view of 14-day stage of Anas. (C) Lateral view, adult stage of Callus (chick). Cartilage = coarse stipple; bone — fine stipple.

(fig. 315D). Each second visceral (hyoid) arch in the shark forms on each side an upper hyomandibula, attached to the otic capsule by fibers of connective tissue, a ceratohyal part, and a lower basihyal element (fig. 315D). The basihyal portion of the two hyoid arches forms a basis for the so-called tongue. The succeeding branchial arches form supports for the gills and develop cartilaginous branchial rays which extend out into the gill area (fig. 315C). Each branchial arch on each side divides into four cartilages, namely, the upper pharyngobranchial, and the lower hypobranchial, the epibranchial and the ceratobranchial elements. The last two elements lie between the first two, and the ceratobranchial element is articulated with the hypobranchial element (fig. 315D).

The visceral skeleton in ganoid and teleost fishes arises similarly to that in elasmobranchs but becomes largely ossified in the adult (fig. 316).

In the frog, the well-developed, visceral skeleton of the late larva becomes greatly modified during metamorphosis and the acquisition of adulthood. The hyoid arch persists in cartilage. The mandibular arch contributes to the formation of the upper and lower jaws. The lower jaw in the metamorphosed frog consists of Meckel’s cartilages, reinforced by membrane bones, the dentaries and the angulospenials. The pterygoquadrate cartilages remain as cartilage and are reinforced by the pterygoid, quadratojugal, squamosal, maxillae and premaxillae, to form the upper jaw (fig. 317B, C and Table 1).

In birds, the first visceral or mandibular arch contributes to the formation of the quadrate and articulare at the angle of the jaw. These two bones on either side represent cartilage bones. (See Table 2.) The hyoid and first branchial-visceral arches form the complicated support for the tongue (consult Table 2).

In mammals, the visceral arches contribute as much to the adult condition as in other higher vertebrates. In the human, the caudal portion of the vestigial upper jaw rudiment persists as the incus, and the caudal portion of Meckel’s cartilage contributes to the formation of the malleus. The mandibular arch thus contributes to the important ear bones (fig. 319C-2). The upper portion of the hyoid arch probably forms the stapes; the ventral portion forms one half of the hyoid bone; and the intervening tissue of the primitive hyoid arch contributes to the formation of the stylohyal structures (fig. 319C, D). The third arch on each side forms the greater horn of the hyoid; the fourth contributes to the thyroid cartilage; the fifth pair forms the arytenoid and cricoid cartilages (fig. 319C and Table 3).

b. Ossification Centers and the Development of Bony Skulls

The formation of the bony crania of all vertebrates entails the use of centers of ossification which involve methods of bone formation previously described. As a rule, one ossification center arises in a single bone, with the exception of those bones, such as the human frontal, sphenoid, or occipital bones, which result from the fusion of two or more bones. In these instances separate centers of ossification are developed in each individual bone. The exact number of ossification centers in all bones has not been exactly determined.

c. Development of the Axial Skeleton

1) Axial Skeleton of the Trunk; a) Notochord. The notochord is one of the basic structural features of the chordate group of animals. It will be recalled (Chapters 9 and 10) that the primitive notochordal band of cells is the physiological instrument which effects much of the early organization of the developing body of the vertebrate embryo. Aside from this basic, apparently universal function in vertebrate development, the notochord later functions as a prominent feature in the development of the median skeletal axis. In the cyclostomatous fishes, a persistent, highly developed notochord, enclosed in elastic, and fibrous, connective-tissue sheaths, is found in the adult. The enveloping, connective-tissue sheaths establish a covering for the nerve cord above and for the blood vessels immediately below the notochord. Vertebrae are not developed, but in the cyclostomes (Petromyzontia) paired cartilaginous rods lie along either side of the nerve cord above (Goodrich, ’30, pp. 27, 28). In the Dipnoi and in the cartilaginous ganoids, such as Acipenser sturio, the notochord persists unconstricted by vertebral elements although supplemented by these structures. In the shark group and in teleost fishes in general, as well as in certain Amphibia, such as Necturus, the notochord is continuous but constricted greatly by the developing vertebral centra. In

Fig. 319. Developmental stages of mammalian neurocranium and splanchnocranium. (A) Human chondrocranium at end of third month viewed from above (from Keibel and Mall, 1910, Manual of Human Embryology, vol. I, after Hertwig’s model). (B) Same, lateral view, slightly modified. (C-1) Lateral view of adult skull showing visceral arch (splanchnocranial) derivatives. (C-2) Auditory ossicles (see fig. 319B). Malleus derived from caudal end of Meckel’s cartilage in lower jaw portion of mandibular visceral arch; incus from caudal end of maxillary process of mandibular arch; stapes from upper or hyomandibular portion of hyoid visceral arch. (D) Lateral view of cat skull and visceral arch (splanchnocranial) derivatives. (E) Human cranium, lateral view, at birth showing fontanels (from Morris, ’42, Human Anatomy, Philadelphia, Blakiston). Cartilage = coarse stipple; bone == fine stipple.

Based largely on data supplied by De Beer, ’37.

Cartilage bones, i.e., bones developed from a Membrane bones, i.e., bones of dermal origin,

Branchial arches on each Branchial arch I (visceral arch III) forms greater horn of hyoid, composed of basibranchial and ceratobranchial bony segments joined by cartilage

Cartilage bones, i.e., bones developed from a Membrane bones, i.e., bones of dermal origin,

poral bone

i. Orbitotemporal region Presphenoid and its orbitosphenoidal wings; Frontal; parietals; palatines; pterygoid

= trabecular region plus basisphenoid and basal areas of its alisphe- processes and squamous portion of alisphe anterior portion of basal noidal wings noidal wings

plate area)

L Nasal (olfactory) capsu- Maxilloturbinal ; elhmoturbinals; cribriform Nasal; lacrimal; vomer; premaxillary and

lar and anterior trabecu- plate ; nasal septum, in part maxillary processes

lar areas

Fig. 320. Diagrams of basic cartilaginous underpinning or foundation of the vertebrat neurocranium. (Somewhat modified from De Beer, ’37, after De Beer and Woodger. (A) Pisces. (B) Placental mammals. It is to be observed that the trabecula cranii ii the fish is represented by the central stem or trabecular plate in the mammal.

most amphibia and in the reptiles, birds, and mammals, the notochord tend: to be entirely displaced by the vertebrae, and its residual remains are restrictet within or between the vertebrae. In mammals, the residual remainder o the notochord constitutes the nucleus pulposus (pulpy nucleus) near th( center of the fibrocartilage of the intervertebral disc. In the human, accordin) to Terry, ’42, p. 288, the pulpy nucleus forms a “pivot round which the bodiei of the vertebrae can twist or incline.”

b) Vertebrae. Vertebrae, the distinct segments of which the spinal columi consists, arise from sclerotomic mesenchyme, derived from the ventro-mesia aspects of the various somites (fig. 252A-D). Potentially, this sclerotomu mesenchyme in each primitive segment becomes segregated into eight masses four on either side of the notochord. These eight masses or blocks of mesen chyme form the arcualia. The arcualia become arranged in relation to th( notochord and the developing intermuscular septa as indicated in figure 321 A These masses are designated as basidorsals and basiventrals, interdorsals anc interventrals. Thus there are two basidorsals, two basiventrals, two interdor sals, and two interventrals.

During the formation of the vertebra in mammals, the sclerotomic masse: within a primitive body segment become associated about the notochorda axis as indicated in figure 321J-L. It is to be observed that the arteries fron the dorsal aorta lie in an intersegmental position. This position represent the area of the myoseptal membrane, shown in figure 321 A. As the sclerotomic masses increase in substance, each mass on each side of the noto chord becomes divisible into an anterior area, in which the mesenchymal cell are less dense, and a posterior area, where the cells are closely aggregated (fig. 321 J). The less dense mesenchymal mass represents the rudiment of the interdorsal vertebral element, while the posterior dense mass of mesenchyme is the basidorsal element. As development proceeds, the basidorsal mass of cells from one segment and the interdorsal mass of the next posterior segment on either side of the notochord move toward each other and align themselves in the intersegmental area as shown in figure 32 IK, L. The basidorsal element thus comes to lie along the anterior portion of the intersegmental area, and the interdorsal rudiment occupies the posterior part of this area. The four vertebral elements, two on either side of the notochord in the intersegmental area, form the basic vertebral rudiments, although rudimentary basiventral and interventral elements possibly are present. The intersegmental artery eventually comes to lie laterally to the forming vertebra.

Once these basic rudiments of the vertebra are established, the vertebra begins to form. In doing so, there is an increase in the number of mesenchymal cells present, and the sclerotomic masses move toward and around the notochord in the intersegmental position. The two dense basidorsal elements from either side expand dorsally around the neural tube as the two interdorsal rudiments coalesce to form the body of the centrum (fig. 321M). Laterally, the rudiment of the rib arises as a condensation of mesenchyme continuous with the forming neural arch and centrum. The rib element continues to grow ventro-laterally, particularly in the thoracic area (fig. 321N). In the lateral growth of the rib rudiment, surrounding mesenchyme is organized and incorporated into the growing structure of the rudiment.

Once the vertebral rudiment is established as a dense mass of mesenchyme, the pre-cartilage stage of cartilage development occurs (fig. 313A). The precartilage stage is followed soon by cartilage (fig. 313B, C). Later, centers of ossification arise as indicated in figure 3210, and the cartilaginous condition becomes converted into a bony condition. Secondary centers of ossification, forming bony epiphyses, ultimately arise after birth at the anterior and posterior ends of each centrum. When the ultimate size of the vertebra is attained, the epiphyseal cartilages between the epiphyses and the centrum of each vertebra become ossified, and the epiphyses thus unite with the centrum. The intervertebral discs of fibrocartilage form in the segmental position between the vertebrae.

It is to be observed that the intersegmental arrangement of the vertebrae permits direct passage of the spinal nerves to the developing musculature within each segment and also permits the musculature of each segment to attach itself to two successive vertebrae. The latter feature is particularly advantageous in lateral bending movements, so prominent in the swimming movements of water-dwelling forms.

See legend, fig. 321, for vertebral development in various vertebrates.

c) Divisions of the Vertebral Column. In fishes, two main divisions of the vertebral column are recognizable, the caudal region where the ver

Fig. 321. Development of vertebrae. The vertebral column in the phylum Vertebrata is a variable structure. In the early embryo the primitive notochord serves as the primitive axis. Later this structure develops fibrous sheaths in fishes and amphibia. The notochord plus its surrounding sheaths serves as the only axial support in the embryo and adult stages of Amphioxiis and Cyclostomes. However, in all true vertebrates, the notochord is supplemented during later embryonic stages by vertebral rudiments known as arcualia (fig. 321, A). Eight arcualia are present typically in each vertebral segment. The arcualia begin as mesenchymal condensations from the sclerotome (see fig. 252, A~D), and later are transformed into cartilaginous masses. In the elasmobranch fishes the cartilaginous arcualia fuse to form the vertebra as described below, but in most vertebrates they undergo ossification.

I. The Formation of Vertebrae in Fishes. In certain instances among the fishes, the arcualia are merely saddled on to the notochord and its sheaths. This condition is found, for example, in the lung fishes and cartilaginous ganoid fishes (fig. 321, E). A vertebral centrum is not developed in these instances.

In the elasmobranch fishes the vertebra is formed essentially from that group of arcualia known as the ba.saiia, that is, the basidorsals and basiveiitraL. These rudiments invade the fibrous sheath from above and below on either side and form the neural arch and centrum as indicated in fig. 321, C. The interbasalia — that is, the intcrdorsals and inlerventrals — lie between the vertebrae. The notochord is constricted greatly in the region of the centrum but is disturbed little in the areas between the centra. That is, the centrum is hollowed out or deeply concave at either end. This form of centrum is found in all amphicoelous vertebrae (fig. 321, P). In the tail region (fig. 321, C'), there are two vertebrae per muscle segment. This condition is known as diplospondyly. Other cartilaginous elements may enter into the formation of the centrum as indicated in fig. 321, C'.

The diplospondylous condition in the tail region of Amia presumably is developed as indicated in fig. 321, H'. In the trunk region of Amia the arcualia associate to form the vertebrae as in fig. 321, H. A certain amount of membrane bone may enter into the composition of the centra in Amia. In the teleost fishes (fig. 321, I), the basidorsals form the neural arches, but the centrum is developed almost entirely from the ossification of fibrpus connective tissue membrane (i.e., membrane bone formation). The basiventrals form the area of attachment of the pleural ribs and also form the hemal arches.,

II. Development of Vertebrae in Amphibia.

In the frog (fig. 321, B), the neural arch of each vertebra appears to arise as the result of fusion and ossification of two basidorsal arcualia. Ossification spreads from the neural arch downward into the developing centrum. The centrum, however, develops as a result of perichordal ossibeation which arises within the membranous connective tissue around the notochord. The rudimentary interdorsals and interventrals probably grow inward into the intercentral spaces to obliterate the notochord between the centra. The interdorsal-interventral complex fuses ultimately with the caudal end of the centrum, to form a rounded knob which articulates with the concave end of the next posterior vertebra. That is, the vertebrae in the frog are procoelous (fig. 321, Q). The urostyle of the frog probably represents a fusion of rudimentary vertebrae caudal to the ninth or sacral vertebra. Vestigial notochordal remains may exist in the center of each bony centrum.

The development of the vertebrae in Necturus (fig. 321, D), resembles that of the frog, with the exception that the bony centrum arises from a perichordal ossification which is entirely independent of the neural arch. Also, the notochord remains continuous, being constricted in the region of the bony centrum, but relatively unconstricted in the area between the centra. That is, the vertebrae are of the amphicoelous type (fig. 321, P). The basiventral arcualia unite to form the hemal arches in the tail.

III. Development of Vertebrae in the Chick and Mammals.

The development of the vertebra in the chick is a complicated affair, as the vertebra is composed of a complex of fused arcualia associated with a perichordal ossification (see fig. 321, F). The vertebrae are heterocoelous, their ends being partly procoelous and opisthocoelous. In mammals vertebrae possess hemal arches and the trunk region without hemal arches but with ribs. The amphibia begin to show a third division, the cervical area or anterior portion of the trunk region in which the vertebrae do not possess ribs. This area is limited to one vertebra, the axis. In the amphibia, also, a sacral region begins to make its appearance. It is only slightly differentiated in waterabiding forms but well developed in the Anura. The caudal vertebral area in the Anura generally is fused to form the coccyx or urostyle. The reptilian vertebral column manifests great variability in the different orders. The turtles show cervical, trunk, and tail regions, with the trunk vertebrae fused with the bony plates of the carapace. In snakes, a short cervical area, a greatly elongated trunk region, and a caudal area are present. Some of the snakes possess the largest number of vertebrae among verterbates, the number reaching several hundreds. Sacral vertebrae are absent in snakes. The lizards and crocodilians show conditions closely resembling the amphibia. In the birds, caudal, synsacral, thoracic, and cervical regions are present, while, in mammals, cervical, thoracic, lumbar, sacral, and caudal regions exist.

d) Ribs. Ribs are not found in cyclostomatous fishes. In the gnathostomes, two types of ribs may be present:

1. dorsal ribs and
2. ventral or pleural ribs.

Fig. 321 — (Continued)

the vertebra appears to arise from two basidorsal and two interdorsal arcualia as indicated in fig. 321, G. The origin of the basidorsal and interdorsal vertebral rudiments from the sclerotomic mesenchyme are shown in figure 321, J-M. The vertebrae are of the acoelous (amphiplatyan) type (fig. 321, S). The chevron bones and hemal arches in the tail region of many mammals represent basiventral elements. Fig. 321, M-O, shows the rib outgrowths from the developing vertebrae. Observe centers of ossification in the vertebra in fig. 321, O.

Fig. 321, A, presents a lateral view of the so-called arcualia in relation to the notochord and the myosepta (myocommata). According to this theory of the development of the vertebrae, the arcualia form the main rudiments from which future vertebrae arise. (B) The adult frog vertebrae showing probable contributions of arcualia. (C and C) Probable contributions of the arcualia to trunk and tail vertebrae of Squalus acanthias. (D) The adult vertebrae of Necturus maculosus. (E) The role played by the arcualia in forming the axial supporting structure in Acipenser sturio. (Redrawn and modified from Goodrich, Vertebrate Craniata, 1909.) (F) The composite origin of the vertebra in the bird. (Redrawn from Piiper, 1928. Phil. Trans. Series B, 216.) (G) Probable con tributions of the arcualia to vertebra formation in man. (H) Probable contributions of the arcualia in the formation of trunk and caudal vertebrae in Amia calva. (I) Same for the teleost, Conodon nobilis. (J-L) The origin and early development of the sclerotomic mesenchyme in the mammal. (M) shows vertebral and costal development in a 15-mm. pig embryo. (N) presents vertebral and costal development in a human embryo of 11 mm. The vertebral and rib rudiments are in the mesenchymal stage at this period. (Redrawn from Bardeen, 1910. Keibel and Mall, Vol. I, Human Embryology, Lippincott, Phila.) (O) is a drawing of developing vertebra in the 22-mm. opossum embryo. (P, Q, R, and S) are diagrams of amphicoelous, procoelous, opisthocoelous and slightly biconcave amphiplatyan (acoelous) vertebrae. (Redrawn and modified from Kingsley, ’25.)

Ribs develop in relation to the basidorsal and basiventral elements and extend outward in the myosepta. The dorsal rib appears typically in the position between the epaxial and hypaxial divisions of the primitive skeletal musculature, whereas the pleural rib lies in close relationship to the coelomic cavity (fig. 31 IB). It is questionable whether or not the hemal arch, when present, is homologous with the ventral or pleural ribs. The shark, Squalus acanthias, has dorsal ribs. This condition is true also of all Tetrapoda. In Amia, the ribs are of the pleural variety, whereas, in most teleosts, pleural ribs are present, supplemented by dorsal or epipleural ribs.

Fig. 322. Development of the sternum in the mammal. (A and C redrawn from Hanson, ’19, Anat. Rec., 17; B redrawn from Kingsley, ’25.) (A) Diagrammatic recon struction of sternum of 24-mm. pig embryo. The two precartilaginous condensations of the mesosternum are united anteriorly with the presternal condensation. The rib or costal condensations are approaching and uniting with the sternal condensations. (B) Schematic representation of sternal rudiments in the mammal. The mesosternal cartilages have segmented into cartilaginous segments or slernebrae. Bilateral centers of ossification arise in each sternebra which later form the bony sternebra. (C) Sternum of old boar, weight 450 lbs. It is to be observed that the sternebrae have remained distinct, and in two of the sternal segments anterior to the xiphisternum the two centers of ossification produce a dual condition within the sternal segment. In the human and certain other mammals the sternebrae fuse to form the gladiolus or corpus sterni.

As indicated above, ribs may be considered as outward extensions or processes of the vertebrae. In the frog, the much-abbreviated ribs become firmly ossified to the basidorsal elements of the vertebrae and extend outward as the transverse processes. However, in most vertebrates, they are articulated with the vertebrae by means of lateral extensions or processes from the vertebrae.

Chondrification of the rib occurs separately from the chondrification of the vertebra, and articulations develop between the rib and the vertebrae (fig. 3210). Similarly, when ossification develops, a separate center of ossification arises in the body of the rib (fig. 3210). However, epiphyseal centers arise in the tubercular and capitular heads, which later unite with the shaft of the rib. The student is referred to Kingsley, ’25, for a full discussion of vertebrae and ribs.

e) Sternum. A sternum connected with the ribs, and thus forming a part of the protective thoracic basket, is found only in reptiles, birds, and mammals. A sternum is absent in the gymnophionan Amphibia (Apoda), is reduced to a midventral cartilaginous series of bars in Necturus, and forms a part of the pectoral girdle in the frog (fig. 323C).

In its formation in the mammal, the sternum begins as a bilateral series of mesenchymal aggregations between the ventro-mesial ends of the clavicular and costal concentrations of mesenchyme (fig. 322A). These mesenchymal aggregations move toward the midline, form pre-cartilage, and then form cartilage. The median cartilaginous mass at the anterior end forms the presternum or episternum; the portion between the rib elements forms the mesosternum, and the posterior free area is the metasternum or xiphisternum (fig. 322B). In forms which have a clavicle, the latter articulates with the episternum. The anterior portion of the mesosternum unites ultimately with the presternum to form the rudiment of the manubrium. The mesosternum segments into blocks or stemebrae, while the caudal free end of the sternum forms the xiphisternum (fig. 322C). Centers of ossification arise in these areas and convert them to bone. In the human, the stemebrae of the mesosternum unite to form the body or corpus sterni, but, in the cat, pig, and many other mammals, they remain distinct.

2) Axial Skeleton of the Tail. The axial skeleton of the tail is modified greatly from that of the trunk region. In water-living vertebrates, the tail forms a considerable portion of the body. As the tail is used for swimming purposes, the contained vertebrae are developed to serve this end. In consequence, rib processes are reduced or lost entirely, and hemal arches for the protection of the caudal blood vessels are strongly developed features. Another feature subserving the swimming function is the tendency toward diplospondyly, i.e., the development of two vertebral centra per segment (fig. 32 IH'). In land forms, the tail tends to be reduced. However, in the armadillo, kangaroo, etc., the tail is a formidable structure, and hemal-arch structures for the protection of blood vessels are developed in the intervertebral area.

Fig. 323. Pectoral and pelvic girdles. (A) Diagrammatic pectoral girdle of Tetrapoda (modified from Kingsley, ’25). (B) Pectoral girdle of Squalus acanthias. (C) Pectoral girdle of the frog, Rana (redrawn from Kingsley, ’25, after Parker). Observe that clavicle is a small bony bar superimposed upon procoracoid; suprascapula removed on right side. (D) Pectoral girdle of the bird. Callus. (E) Human pectoral girdle. (F) Diagrammatic representation of pelvic girdle in Tetrapoda (modified from Kingsley, ’25). (G) Pelvic girdle in Squalus acanthias. (H) Pelvic girdle in Rana cateshiana. (1) Pelvic girdle in Callus (chick). (J) Pelvic girdle in human. (K) Pelvic girdle in Didelphys (opossum). (L) Dorsal view of sacrum and pelvic girdle in the armadillo, Tatusia.

d. Development of the Appendicular Skeleton of the Paired Appendages

1) General Features. Two types of appendages are found in the vertebrate group:

1. median unpaired appendages which take their origin in the median plane and
2. paired bilateral appendages which arise from the lateral surface of the body.

Median appendages appear in the fishes, aquatic urodeles, and. in the larval form of anuran amphibia. They also occur in the crocodilian and lizard groups, among the reptiles, and, among mammals, in the whales.

All appendages arise as outgrowths of the body. The median appendages or fins of fishes possess separate skeletal structures for support, but the median, fin-like structures in the tails of amphibia, reptiles, and whales do not acquire a separate internal skeleton. All fishes possess a median caudal or tail fin at the terminus of the tail, a median anal fin posterior to the anal area, and one or more median dorsal fins.

Most vertebrates possess two pairs of bilateral appendages (Chap. 10, p. 508), one pair located anteriorly in the pectoral or breast region and the other pair situated posteriorly in the pelvic area just anterior to the anus. Each paired appendage has a skeleton composed of two parts:

1. a girdle component and
2. a limb component.

The girdle component of each appendage is associated with the axial skeleton of the trunk and also with the girdle component of the appendage on the contralateral side. The entire girdle of each pair of appendages thus tends to form a U-shaped structure with the closed portion placed ventrally (fig. 323 A-K). In fishes, the open dorsal area of the U-shaped girdle in the pectoral area may be closely associated with the axial skeleton, but, in land forms, it is the pelvic girdle which joins the axial skeleton. This relationship is to be expected, for, in fishes, the tail is the more important propulsive mechanism, the head region being the “battering ram” insinuating itself through the water. As a result, the skull, anterior vertebrae, and the pectoral girdle ofttimes form a composite structure as, for example, in many teleost fishes. In land-living vertebrates, on the other hand, the main propulsive force is shifted anteriorly from the tail region and is assumed to a great extent by the posterior pair of appendages. In consequence, the pelvic girdle acquires an intimate relationship with the axial skeleton, and a fusion of vertebrae to form the sacrum occurs. The sacrum serves as the point of articulation between the pelvic girdle and the axial skeleton and is most highly developed in those species which use the hind limbs vigorously in support and propulsion of the body (fig. 3231, L).

Two main types of bilateral appendages are found in the vertebrate group:

1. the ichthyopterygium of Pisces and
2. the cheiropterygium of Tetrapoda.

The former is flattened dorso-ventrally, and assumes the typical flipper or fin shape, while the latter is an elongated, cylindrical affair.

2) Development of the Skeleton of the Free Appendagk^The paired appendages arise either as a dorso-ventrally flattened fold of the epidermal portion of the skin, or as a cylindrical outgrowth of the epidermis. (See Chap. 10.) Within the epidermal protrusion, is a mass of mesenchyme (figs. 262D, E; 324A). As development proceeds, condensations of mesenchyme, centrally placed, begin to foreshadow the outlines of the future skeletal structures of the limb (fig. 324A, C, D). This mesenchyme gradually becomes more compact to form a pre-cartilage stage, to be followed by a cartilaginous condition.

The pattern, which these cartilages of the limb assume, varies greatly in the two types of limbs mentioned above. In the ichthyopterygium (fig. 323B, G), they assume a radially arranged pattern, extending out from the point of attachment to the girdle, whereas, in the cheiropterygium (fig. 323A), they assume the appearance characteristic of the typical limb of the Tetrapoda.

In the tetrapod limb, such as that of the hog, chick, or human, elongated, cylindrically shaped bones begin to make their appearance in mesenchyme (fig. 324A-E). Following the cartilaginous condition, a center of ossification arises in the shaft or diaphysis of each developing bone, transforming the cartilage into bone (figs. 314E, F; 324E). Cancellous or spongy bone is formed centrally within the shaft, while compact bone is deposited around the periphery of the shaft (fig. 314E, F). Later, the cancellous bone of the shaft is resorbed, and a compact bony cylinder, containing a relatively large marrow cavity, is formed. Separate centers of ossification, the epiphyses, arise in the distal ends of the bones (fig. 3241). Each epiphysis is separated from the bone of the shaft by means of a cartilaginous disc, the epiphyseal cartilage (fig. 3241). At maturity, however, the bony epiphysis at each end of the bone becomes firmly united with the shaft or diaphysis by the appearance of an ossification center in the epiphyseal cartilage (fig. 324J). Internally, the ends of the long bones tend to remain in the cancellous or spongy condition, whereas the shaft is composed of compact bone with an enlarged central marrow cavity (fig. 324J). For later changes of the bony substance involved in the growth of bone, see growth of bone, p. 693.

3) Formation of the Girdles. The typical tetrapod pectoral girdle (fig. 323 A) is composed of a sternal midpiece, three lateral columns, extending dorsad from the sternal area on either side, the clavicle, procoracoid, and coracoid to which is attached dorsally the scapula. Often a suprascapula is attached to the scapula. The pelvic girdle of the Tetrapoda, on the other hand (fig. 323F), is composed of two lateral columns on either side. The anterior column is called the pubis, and the posterior column is the ischium. An ilium is attached to the dorsal ends of the pubis and ischium on either side. Epipubic and hypoischial midpieces are sometimes present at the midventral ends of the pubic and ischial columns in some species.

Fig. 324. Development of long bones of the appendages. (B and E have been modified to show conditions present in the fore- and hind appendages at about 8 weeks. For detailed description of limb development consult Bardeen, ’05, Am. J. Anat., 4; Lewis, 02, Am. J. Anat., 2.) (A) Forelimb at II mm. (B) Forelimb at about eighth week, showing centers of OKSsification in humerus, radius and ulna. (C) Hindlimb at 11 mm. (D) Hindlimb at 14 mm. (E) Hindlimb at about eighth week, showing centers of ossification in femur, tibia, and fibula. The heavy strippling in A, C, D represent centers of chondrification; the black areas in B and E portray ossification centers within cartilaginous form of the long bones. F-J represent stages in joint development.

As in the development of the skeleton of the free appendage, all the rudiments of these structures are laid down in cartilage and later ossify, with the exception of the clavicle which may be of intramembranous origin (Hanson, ’20a and ’20b). The clavicles are more strongly developed in man, whereas the coracoidal elements are vestigial (fig. 323E). In the cat, the coracoidal and clavicular elements are reduced. However, in the chick and frog, the coracoidal elements are dominant (fig. 323C, D). In the pelvic girdle, the iliac, pubic, and ischial elements are constant features in most Tetrapoda. In the shark, a single coracoid-scapula unit is present in the pectoral girdle and the pelvic girdle is reduced to a small transverse bar of cartilage (fig. 323B, G).

e. Growth of Bone

Bone once formed is not a static affair, for it is constantly being remodeled and enlarged during the growth period of the animal. In this process, bone is destroyed arid resorbed by the action of multinucleate giant cells, called osteoclasts, or specialized, bone-destroying cells and is rebuilt simultaneously in peripheral areas by osteoblasts from the surrounding periosteal tissue.

To understand the processes involved in bone growth, let us start with the conditions found in the primitive shaft of a long bone (fig. 314F). Within the bony portion of the shaft, there is a network of cancellous bone, and, peripherally, there are lamellae of compact bone. The following transformative activities are involved in the growth of this bone:

1. Within the bone, the cancellous columns of bony substance are destroyed by osteoclasts, the bony substance is resorbed, the marrow spaces are enlarged, while, peripherally, circumferential lamellae are deposited around the bones beneath the periosteum.
2. Distally, cartilage is converted into cancellous bone while outer circumferential lamellae are fabricated beneath the periosteum. The bony substance thus creeps distally, lengthening the shaft of the bone.
3. As the bone increases in length, some of the bony substance, forming the wall of the shaft or diaphysis is destroyed. This alteration is effected to a degree by vascular buds which grow into the bony substance from the periosteum around the outer surface of the bone and from the endosteum which lines the marrow cavities. These vascular buds erode the bony substance with the aid of osteoclasts and produce elongated channels in the bone, channels which tend to run lengthwise along the growing bone. Once these channels are made, osteoblasts lay down bony lamellae in concentric fashion, converting the channel into an Haversian system. (Consult Maximow and Bloom, ’42, pp. 141-145.) The Haversian systems thus tend to run parallel to the length of the bone. The Haversian canals open into the central marrow cavity of the bone in some of the Haversian systems, whereas others, through Volkmann’s canals, open peripherally.
4. While the foregoing processes are in progress, circumferential lamellae are laid down around the bone. The bone’s diameter thus grows by the erosion of its bony walls (including previously established Haversian systems) and by the formation of new bony substance externally around the diaphysial area which is destroyed and resorbed. New Haversian systems and new circumferential lamellae in this way supersede older systems and lamellae.

At the distal ends of the bone within the spaces of the cancellous bone, red marrow is found. In the shaft or diaphysis, however, the contained marrow cavity is filled with yellow bone marrow, composed mainly of fat cells.

The distal growth of elongated, cylindrically shaped bones, such as the phalanges or the long bones of the limbs, is possible, while epiphyseal cartilage remains between the shaft of the bone and the bony epiphysis at the end of the bone. The maintenance and growth of the epiphyseal cartilage is prerequisite to the growth of these bones, for the increase in the length of the bony shaft involves the conversion of cartilage nearest to the bony shaft into cancellous bone. A bony cylinder of compact bone is then formed around the cancellous bone. When, however, the epiphyseal cartilage ceases to maintain itself, and it in turn becomes ossified, uniting the epiphysis to the bony shaft, growth of the bone in the distal direction comes to an end. Growth in the length of a vertebra also involves the epiphyseal cartilages lying between the bony ends of the centrum and the epiphyses. Increase in size of the diameter of the vertebra results from the destruction and resorption of bone already formed and the deposition of compact bone around the periphery.

In the case of flattened bones of cartilaginous origin such as the scapula or the pelvic-girdle bones, growth in the size of the bone is effected by the conversion of peripherally situated cartilage into bone, and by the destruction and resorption of bone previously formed and its synchronous replacement external to the area of destruction. On the other hand, in the growth of flat bones of membranous origin, the bone increases in size along its margins at the expense of the connective tissue surrounding the bone. Growth in the diameter of membrane bones is similar to that of cartilage bone, namely, destruction, resorption, and deposition of new bone at the surface.

. Formation of Joints

1) Definitions. The word arthrosis is derived from a Greek word meaning a joint. In vertebrate anatomy, it refers to the point of contact or union of two bones. When the contact between two bones results in a condition where the bones actually fuse together to form one complete bone, the condition is called ankylosis or synosteosis. If, however, the point of contact is such that the bones form an immovable union, it is called a synarthrosis; if slightly movable, it forms an amphiaithrosis; and where the contact permits free mobility, it is known as a diarthrosis. Various degrees of rapprochement between bones, therefore, are possible.

2) Ankylosis (Synosteosis) and Synarthrosis. In the development of the bones of the vertebrate skull, two types of bone contact are effected:

(1) ankylosis and

(2) synarthrosis.

In the human frontal bone, for example, two bilaterally placed centers of ossification arise in the connective-tissue membrane, lying below the skin in the future forehead area. These two centers increase in size and spread peripherally until two frontal bony areas are produced, which are separated in the median plane at birth. Later on in the first year following birth, the two bones become sutured (i.e., form a synarthrosis) in the midsagittal plane. Beginning in the second year and extending on into the eighth year, the suture becomes displaced by actual fusion of bone, and ankylosis occurs. In the cat, however, the two frontal bones remain in the sutured condition (synarthrosis). The temporal bone in the human and other mammals is a complex bone, arising by the ultimate fusion (ankylosis) of several bones. In the human at birth, three separate bones are evident in the temporal bone:

(1) a squamous portion,

(2) a petrous portion, and

(3) a tympanic part.

The squamous and the tympanic bones are of membranous origin, whereas the petrous portion arises through the ossification of the cartilaginous otic capsule. The fusion of these three bones occurs during the first year following birth. The occipital bone is another bone of complex origin. Five centers of ossification are involved, viz., a basioccipital, two exoccipitals, a squamous inferior, and a squamous superior. The last arises as a membrane bone; the others are endochondral. Ultimate fusion of these entities occurs during the early years of childhood and is completed generally by the fourth to sixth years. In the cat, the squamous superior remains distinct as the interparietal bone. Finally, the sphenoid bone in the human represents a condition derived from many centers of ossification. According to Bardeen, TO, fourteen centers of ossification arise in the sphenoidal area, ten of them arising in the orbitotemporal region of the primitive chondrocranium. At birth, two major portions of the sphenoid bone are present, the presphenoid and the basisphenoid, being separated by a wedge of cartilage. Ultimate fusion of these two sphenoid bones occurs late in childhood (Bardeen, ’10). In the adult cat, they remain distinct. The maxillary bone in the human arises as a premaxillary and a maxillary portion; later these bones fuse to form the adult maxilla. In the cat, on the other hand, these two bones remain distinct. (Consult also Table 3.)

The history of the human skull, therefore, is one of gradual fusion (ankylosis) of bones. In many parts, however, fusion does not occur, and definite sutures (synarthroses) are established between the bones, as in the case of the two parietals, the parietal and the occipital, the frontal and the parietals, etc.

The formation of the association between the parietal bones and neighboring bones establishes an interesting developmental phenomenon, known as the fontanels. The fontanels are wide, membranous areas between the developing parietal and surrounding bones which, at birth, are not ossified. These membranous areas are the anterior fontanel, in the midline between the two parietals and two frontal bones, and the posterior fontanel, between the parietals and the occipital bones. The lateral fontanels are located along the latero- ventral edges of the parietal and neighboring bones (fig. 319E).

3) Diarthrosis. A diarthrosis or movable joint is established at the distal ends of the elongated, cylindrically shaped bones of the body. Diarthroses are present typically in relation to the bones of the appendages. As the bones of the appendages form, there is a condensation of the mesenchyme in the immediate area of the bone to be formed. At the ends of the bone, the mesenchyme is less dense than in the area where the rudimentary bone is in the process of formation (fig. 324A-E). As a result, the area between bones is composed of mesenchyme less compact and less dense than in the areas where bone formation is initiated (fig. 324F, G). This mesenchyme at the ends of the bones thus forms a delicate membrane, tying the bony rudiments together, and, as such, forms a rudimentary synarthrosis. As development proceeds, the miniature bone itself becomes more dense, and, eventually, cartilage is formed. The latter later is displaced gradually by bone (fig. 324E). The areas between the ends of the respective developing bones become, on the contrary, less dense, and a space within the mesenchyme is developed between the ends of the forming bones (fig. 324H). As this occurs, connective tissue, continuous with the periosteum, forms around the outer edges of the ends of the bones, tying the ends of the bones together (fig. 324H, I). A cavity, the joint cavity, thus is formed at the ends of the bones, bounded by the cartilage at the ends of the bones and peripherally by connective tissues or ligaments which tie the ends of the bones together along their margins. The membrane which lines the joint cavity is known as the synovial membrane, and the cartilaginous discs at the ends of the bones form the articular cartilages (fig. 324H, J).

4) Amphiarthrosis. The term amphiarthrosis refers to a condition intermediate between synarthrosis and diarthrosis. This condition occurs for example in the area of the pubic symphysis.

g. Dermal Bones

As observed in figure 31 lA, the primitive mesenchyme of the ghost skeleton of the embryo underlies the epidermal tube, as well as enmeshing the neural, gut, and coelomic tubes. As mentioned previously, wherever mesenchyme exists, a potentiality for bony or bone-like structures also exists. Consequently, it is not surprising that various types of dermal armor or exoskeletal structures in the form of bone, dermal scales, and bony plates are developed in various vertebrates in the dermal area, as described in Chapter 12. Aside from the examples exhibited in Chapter 12, other important bony contributions to the skeleton of vertebrates may be regarded as essentially dermal in origin. Among these are the membrane bones of the skull (Tables 1, 2, and 3 ) . These bones sink inward and become integrated with the basic chondrocranial derivatives to form a part of the endoskcleton. Other examples of membrane bones of dermal origin are the gastralia or abdominal ribs of the Tuatera (Sphenodon) and the Crocodilia, the formidable, dermal, bony armor of the Edentata, e.g., the armadillo, and the bony plates on the head, back, and appendages in certain whales (Kingsley, ’25, p. 17). All these examples of dermal armor or exoskeletal structures form an essential protective part of the entire hard or bony skeleton of vertebrate animals.

Bibliography

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