Book - Developmental Anatomy 1924-10

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Arey LB. Developmental Anatomy. (1924) W.B. Saunders Company, Philadelphia.

   Developmental Anatomy 1924: 1 The Germ Cells and Fertilization | 2 Cleavage and the Origin of the Germ Layers | 3 Implantation and Fetal Membranes | 4 Age, Body Form and Growth Changes | 5 The Digestive System | 6 The Respiratory System | 7 The Mesenteries and Coelom | 8 The Urogenital System | 9 The Vascular System | 10 The Skeletal System | 11 The Muscular System | 12 The Integumentary System | 13 The Central Nervous System | 14 The Peripheral Nervous System | 15 The Sense Organs | C16 The Study of Chick Embryos | 17 The Study of Pig Embryos | Figures Leslie Arey.jpg
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Chapter X The Skeletal System

1. Histogenesis of the Supporting Tissues

Connective tissue, cartilage, and bone all differentiate from that type of diffuse mesoderm known mesenchyme (Fig. 3). Mesenchyme arises directly from the primitive streak, and secondarily from mesodermal segments and the lateral somatic and splanchnic layers (Fig. 211). It is a spongy mesh work composed of branching and anastomosing cells; between these occur open spaces filled with a ground substance of coagulable fluid. In early embryos the mesenchyme constitutes an unspecialized packing material between the external and internal epithelia (Fig. 212), but it soon differentiates into various tissues and organs (p. 7). (jf these, the inert supporting tissues are peculiar in that a fibrous, hyaline, or calcified matrix forms, which becomes bulkier than the persisting cellular elements. In each type the origin of such matrix, whether inter- or intracellular, is disputed.

Connective Tissue Discordant views exist as to the precise manner in which connectivetissue fibers differentiate. Some maintain that the fibrils develop within the cytoplasm of mesenchyme cells and are subsequently extruded into the adjoining matrix. A modification of this theory, proposed by Mall, traces the origin of the fibrils to a hyaline, ectoplasmic layer of the syncytial mesenchyme; this layer then transforms into matrix, while the nuclei and granular endoplasm remain unaffected as definitive connective-tissue cells.

A rival theory, strongly supported of late, interprets the primitive matrix as a lifeless, gelatinous ground substance, secreted by the mesenchyme. In it fibers are formed by a gradual process of organization, which, according to Baitsell (iq2i), is structurally identical with the transformation of a plasma clot into fibrin.

Reticular Tissue. - Except for the jelly-like mucous tissue of the umbilical cord, reticular tissue departs least from the embryonal type. The fine reticular fibrils remain embedded within the cytoplasm of the cells (Downey, 1922).

White Fibrous Tissue. - The differentiation of this tissue may be divided into two phases: (i j a prefibrous stage, marked by the appearance of fibrils resembling those of reticular tissue (Fig. 203, at top); (2) the fibrils take the form of parallel bundles and are converted, through a chemical change, into typical white fibers (Fig. 203, at middle). The early, spindle-shaped cells transform into the several types characteristic of the adult. In areolar tissue, the bundles of white fibers are interwoven to form a meshwork; in tendon, ligaments, and fascias they are arranged in compact, parallel fascicles.


Fig. 203. - The differentiation of white fibers in the Fig. 204. - The differentia skin of a 5 cm. pig embryo (after Mall). X 270. tion of elastic fibers in the umbilical cord of a 7 cm. pig embryo (after Mall). X 270.

Elastic Tissue. - Yellow elastic fibers develop in association with the white variety (Fig. 204). They originate singly after the general manner of white fibers, but may coalesce, as in the fenestrated membranes of arteries.

Adipose Tissue

Certain of the mesenchymal cells give rise, not to fibroblasts, but to fat cells. They secrete within their cytoplasm droplets I of fat which increase in size and become confluent (Fig. 205). Finally, a single globule fills the cell, and the nucleus and cytoplasm are pressed to the periphery. Fat cells are most numerous along the course of blood vessels in areolar tissue and appear first during the fourth month In several locations there are groups of distinctive, granular lipoblasts, termed adipose glands, but at infancy they become indistinguish- I able from the ordinary fat cells.


Fig. 206. - Two interpretations of the development of cartilage (Lewis and Stohr). . 1 , Studnicka; B, Mall.


A preliminary stage in the development of cartilage begins as early as the fifth week with the enlargement of mesenchymal cells to form a - compact, cellular tiSsue, designated prccartilage (Fig. 206). The origin of matrix is interpreted in two ways: (i) Some claim that it appears between the cells from thickened and transformed ectoplasmic walls (Fig. 206 A). (2) According to Mall, mesenchymal cells give rise first to an ectoplasm in which fibrillce develop. Next, the cells increase in size and are gradually extruded until they lie in the intercellular spaces (Fig. 206 B). Simultaneously, the ectoplasm undergoes both a chemical and structural change and is converted into the hyaline matrix peculiar to cartilage.

The matrix of hyaline cartilage remains homogeneous. In fibro- i cartilage, white fibers also are dejjosited within the matrix, in elastic f cartilage, yellow elastic fibers. Cartilage grows both internally and • externally. Interstitial growth results from the proliferation of cartilage cells and the production of new matrix by them. Ap positional growth takes place through the mitotic activity of the connective-tissue sheath, y the perichondrium; its inner cells are transformed into young cartilage cells.


Bone begins to appear after the sixth week. There are two types: the membrane bones of the face and cranium which develop directly within fibrous sheets, and the cartilage bones which replace the earlier cartilaginous skeleton. The mode of histogenesis, however, is identical in each. Bone matrix forms through the activity of specialized, connective-tissue cells, named osteoblasts (bone-formers). First, fibrilla2 and then interfibrillar lime salts differentiate (Fig. 207). Whether these constituents '. are transformed ectoplasm or intercellular deposits is debated.

Development of Membrane Bone. - The flat bones of the face and cranial vault are preceded by connective-tissue membrane. At one â–  I or more central points intramembranous ossification begins. Such centers of ossification are characterized by the appearance of osteoblasts which ; promptly deposit bone matrix in the form of spicules (Fig. 207 A). These | unite into a mesh work of trabeculjc that spreads radialty in all directions. :i Since the osteoblasts are arranged in an epithelioid layer upon the surface J of a spicule, the latter grows both in thickness and at its tip (Fig. 207). as the matrix is progressively laid down, some osteoblasts become trapped and remain imprisoned as bone cells; these are lodged in spaces termed lacunae.

Somewhat later, the mesenchyme next; the flat surfaces of the spongy plate thus formed condenses into a fibrous membrane, the periosteum (Fig. 207 B). Osteoblasts arise on its inner surface and deposit parallel lamellte of compact bone. This process is known as periosteal ossification In such a manner are developed the dense inner and outer tables, joined by the spongy diploe already described.

Fig. 207. - Two stages in the development of bone. . 4 , Section through the frontal bone of a 20 mm. pig embryo (after Mall). X 270. B, Section through the periosteum and bone lamellse of the mandible of a three-months - fetus (Prentiss). X 325.

Much bone that is first formed is provisional, and so is resorbed and replaced in varying degrees as the bone grows and assumes its final modelling. At this time, large, multinucleate cells appear upon the surface of the bone matrix (Fig. 207 B). These giant cells are named osteoclasts, that is, bone destroyers. There is, however, no positive evidence that the osteoclasts are responsible for bone dissolution; more likel}^ they are degenerating, fused osteoblasts and freed bone cells (Arey, 1920). The open spaces of spongy bone are filled with derivatives of the mesenchyme. Such reticular tissue, fat cells, blood vessels, and developing blood cells constitute the red hone marroiv.

Development of Cartilage Bone

The shape of a cartilage bone is determined by the transitory cartilage model which precedes it (Fig. 209). The chief peculiarity of this method of bone formation is the preliminary destruction of the cartilage. For this reason, these skeletal elements are often designated replacement bones. Thereafter, the course of events is essentially as in the development of a membrane bone. Ossification occurs both within the eroded cartilage and peripherally beneath its perichondrium (Fig. 208). In the first case, the process is intracartilaginous or endochondral, in the second instance, perichondral, or better, periosteal.

Endochondral Bone Formation

In the center of the cartilage the cells enlarge, become arranged in characteristic radial rows, and lime is deposited in their matrix (Fig. 208). The cartilage cells and part of the calcified matrix then disintegrate and disappear, thereby forming primordial marrow cavities. This destruction apparently is caused by the vascular primary marrow tissue which simultaneously invades the cartilage. It arises from the inner, cellular layer of the perichondrium and burrows into the cartilage in bud-like cords. Such eruptive tissue gives rise to osteoblasts and bone marrow which occupy the primordial marrow cavities. The osteoblasts first de])osit matrix directly upon persisting spicules of cartilage, hence endochondral bone is spongy. Similarly, the hitherto intact regions of the cartilage undergo progressive invasion, destruction, and replacement until eventually the entire cartilage is superseded by cancellous bone.

.Periosteal Bone Formation. - While the foregoing changes are occurring within the cartilage, compact bone develops about it (Fig. 208). This process is identical with the formation of the tables of the flat bones, and likewise is due to the activity of the inner osteogenetic layer of the perichondrium which now converts directly into the periosteum. Those bone lamelkv deposited about blood vessels that course in hollowed grooves are concentrically arranged into Flaversian systems.

.Growth of Bones. - Flat membrane bones increase in lateral extent by continued marginal ossification from osteoblast-rich connective tissue at the site of the later sutures. Both cartilage and membrane bones grow in thickness by the further deposition of periosteal matrix. In a long bone, this superficial accretion is accompanied by a central resorption which destroys not only the endochondral osseous tissue but also much of the earlier periosteal layers. As a result, cancellous bone, and its associated red bone marrow, persist only at the ends, whereas in the middle region an extensive open cavity develops. The latter is filled with yellow bone marrow, composed chiefly of fat cells.


Zone of cartilage erosion and endochondral ossification .

^ Zone of calcified cartilage I (Cells swollen and in rows) .

â– j! .

/ Zone if unmodified cartilage .

- Level of diarthroidal joint anlage .

Periosteal bone .

Marrow cavity .

Endochondral hone deposited OH remains of cartilage .

Position of later epiphysis .

Fig. 208. Cartilage bone development as illustrated in the finger of a five-months - fetus (Sobotta). X 15. Longitudinal section.


J .


2u .

Most bones, especially those preformed in cartilage, have more than one center of ossification (Fig. 209). In all, there are over 8co such centers, half of which first appear after birth. On the average, therefore, there are four centers to each mature bone. Many cartilage bones, such as occur in the extremities, vertebree and ribs, lack periosteum on their articular surfaces. The consequent inability to increase in length by ordinary means has led to an interesting adaptation. The cartilage at either end grows rapidly, and progressively ossifies, but sometime between birth and puberty, or even later, osteogenetic tissue invades these cartilages and secondary ossification centers, the epiphyses, are established (Fig. 209 C, D). Both surfaces of the intervening cartilaginous plate continue to develop new cartilage as long as the bone lengthens, and this in turn is steadily replaced by bone matrix. Finally, when the adult length is attained, the cartilage ceases proliferation, ossifies, and, the epiphyses are .


Fig. 209. - Diagrams to illustrate the method of growth in a long bone (Prentiss).


firmly united to the central mass. The so-called epi physeal lines mark this union.

.Joints. - The joints occur at regions where the original mesenchyme fails to differentiate into skeletal elements. Such articulations include two general groups; (i) synarthroses, in which little movement is allowed; (2) diarthroses, or freely movable joints.

In joints of the synarthroidal type, the mesenchyme differentiates into a uniting layer of connective-tissue {suture, syndesmosis) or cartilage {synchondrosis) .

Diarthroidal joints are characterized by a prominent joint cavity, between the movable skeletal parts, and a ligamentous capside at the periphery (Fig. 210 B). The joint cavity arises from a cleft in the open mesenchyme; the capsule from the denser external tissue continuous with the periosteum (Figs. 208 and 210). The cells on the inner surface of the capsule flatten into the epithelioid synovial membrane. Ligaments or tendons which apparently course through the adult joint cavities represent .

212 .


secondary invasions, covered with reflexed synovial membrane, and hence are really external to the cavity. Sesamoid bones develop in relation to tendons, and, usually, joints; they commonly arise in the substance of the primitive joint capsule and may exhibit a cartilaginous stage.


Cartilage Joint cleft Perichondrium Mesenchyme .

Marrmv cav Synovial membrane Joint cavity Artictdar cartilage Joint ca psnle Spongy bone Periosteum Compact bone .

Fi(', 2 10. - Stages in the development of a diarthroidal joint.


u. MORPHOGENESIS OF THE SKELETON The skeleton comprises: (i) the axial skeleton (skull, vertebrae, ribs, and sternum), and (2) the appendicular skeleton (pectoral and pelvic girdles and the limb bones). Except for the flat bones of the face and cranial vault, the l)ones of the mammalian skeleton exhibit first a blastemal, or membranous stage, next a cartilaginous phase, and Anally a permanent, osseous condition. A comparalole ascending series occurs among adult chordates of the present day. It seems that the bones of the higher vertebrates that are descended from the cartilaginous skeleton of Ashes pass through a reminiscent cartilaginous stage, whereas those additional bones made necessary by the increased size of the brain develop directly in membrane.

THE AXIAL SKELETON The primitive axial support of all vertebrates is the notochord, or chorda dorsalis, the origin of which has been traced on ])p. 40 and 42. The notochord constitutes the only skeleton of Amphioxus, whereas in Ashes and amphibians it is replaced in part, and in higher animals almost entirely, by the permanent axial skeleton. Among mammals, this supporting rod is transient, except at the intervertebral discs where it persists as the nuclei pitlposi.

The axial skeleton differentiates from mesenchyme, most of which comes from the adjacent pairs of mesodermal segments. Toward the .


213 .


Somatic 7nesoderm .

Splanchnic 7)t€Soderm .

Fig. 21 1. - Transverse section of a 4.5 mm. human embryo, showing the development of the sclerotomes (Kollmann). X about 300.


Spinal ganglion .

Dermatome (?) .

M votome .

Spinal nerve .

Arm bud .

Proliferating cells of myotome .

Mesonephric duct Mesonephric tubule and glomerulus Ccelom Somatic mesoderm .


- S ® a ®9 4 

s'a Q 6 Q 0a Of 99 I ® Q .

Fig. 212. - Transverse section of a 10.3 mm. monkey embryo, showing the sclerotome, myotome and dermatome (Kollmann). A, aorta; *, sclerotome.


214 .


end of the third week, their temporary cavities fill with diffuse, spindleshaped cells, derived from the surrounding walls (Fig. 21 1). The median side of the segment then opens and its mesenchymal content, designated a sclerotome, migrates mesad (Fig. 212). The sclerotomes are the anlages of verte!:>ra2 and ribs.

The Vertebrae and Ribs.- -The sclerotomic mesenchyme comes to lie in paired segmental masses on either side of the notochord, separated from similar masses before and behind by the intersegmenial arteries (Fig. 212). In embryos of about 4 mm., each sclerotome differentiates into a caudal, compact portion and a cranial, less dense half (Fig. 213 A). From the caudal portions, horizontal tissue masses now grow toward the median plane and enclose the notochord, thus establishing the body of each vertebra (Figs. 123 and 214). Similarly, dorsal extensions pass dorsad around the neural tube to form the vertebral arch, and ventro-lateral outgrowths constitute the costal processes. The looser tissue of the cranial halves .

Fig. 213. - Frontal sections through the left mesodermal segments of human embryos. A, at about 4 mm., showing the differentiation of the sclerotomes into less dense and denser regions; B , at about 5 mm., illustrating the union of the halves of successive sclerotomes to form the anlages of the vertebne.

.also grows mesad and fills in the intervals between successive denser regions.

The denser, caudal half of each sclerotomic mass presently unites with the less dense, cranial half of the sclerotome next caudad to form the anlages of the definitive vertebra: (Fig. 213 B). Mesenchymal tissue, filling the new intervertebral fissure thus formed, gives rise to the intervertebral discs. Since a vertebra is formed from parts of two adjacent sclerotomes, it is evident that the intersegmental artery must now pass over the body of a vertebra, and the myotomes and vertebra alternate in position.

.Following this blastcmal stage, centers of chondrification appear, two centers in the vertebral body, one in each half of the vertebral arch, and one in each costal process (Fig. 214). These centers enlarge and fuse into a solid cartilaginous vertebra. The original union of the costal processes, which will give rise to ribs, with the vertebral body is temporary, for an .


â– T i â– â– â– â–  Notochord Hi' I ,> A nlage of vertebra it 'â– 'â– i:. $,. Intervertebral fissure C-i i ^ - Intersegmental artery .

B .


215 .

articulation next the head develops subsequently. T ransverse and articular processes grow out from the vertebral arch, and the rib cartilages, having in the meantime formed tubercles, articulate with the transverse processes somewhat later. The various ligaments of the vertebral column arise from mesenchyme surrounding the vertebree.

.Finally, at the end of the eighth week, the stage of ossification sets in (Fig. 222). A single center appears in the body, one in each half of the arch, and one near the angle of each rib. The replacement of cartilage by bone is not completed until several years after birth. At about the seventeenth year, secondary centers arise in the cartilage still covering the cranial and caudal ends of the vertebral body and form the disc-like, bony epiphyses. These unite with the vertebra proper to constitute a single mass at about the twentieth year.


Neural tube .


Fig. 214. - Transverse section through the blastemal stages of vertebra and ribs from a 13 mm. human embryo (partly after Bardeen). X 18. The light areas are centers of chondrification.


While the foregoing account holds for vertebrae in general, a few' deviations occur. When the atlas is formed, a body differentiates as w'ell, but it is appropriated by the body of the epistropheus (axis), thereafter serving as the tooth-like dens of the latter. The sacral and coccygeal vertebrae represent types wdth reduced vertebral arches. At about the tw'entyfifth year the sacral vertebrae unite to form a single bony mass, and a similar fusion occurs between the rudimentary coccygeal vertebra.

The ribs originate in the costal processes wTich are ventro-lateral outgrow - ths from the vertebral bodies (Fig. 214). Each has an early center of chondrification and ossification (Fig. 222). About puberty, two epiphyseal centers appear in the tubercle and one in the head. The highest development of ribs is realized in the thoracic region. In the cervical region they are short; their tubercles fuse wdth the transverse processes and their heads wfith the vertebral bodies, thus leaving intervals, the transverse foramina, through wTich the vertebral vessels course. In the lumbar region, the ribs are again diminutive and are fused to the trans.


216 verse ])rocesses. The rudimentary ribs of the sacral vertebras are represented by flat plates which unite on each side to form a pars lateralis of the sacrum, (Inly in the first of the coccygeal vertebrae are there traces of ribs.

The Sternum. -Modern studies prove that the sternal anlages arise as paired mesenchymal bands, with which the first eight or nine thoracic ribs fuse secondarily. After the heart descends into the thorax, these cartilaginous sternal bars, as they now may be termed, unite in a craniocaudal direction to form the sternum, at the same time incorporating a smaller, mesial sternal anlage (Fig. 215). Ultimately, one or two pairs of the most caudal ribs lose their sternal connections, the corresponding .


Fig. 215. - The sternum of a human fetus Fig. 216. - Sternum of a child, showing centduring the third month. ers of ossification.

.portion of the sternum constituting the xiphoid process in part. At the cranial end of the sternum there are two imperfectly separated episternal cartilages with which the clavicles articulate. These usually unite with the longitudinal bars and contribute to the formation of the manubrium. Variations in the ossification centers are not uncommon, although a primitive, bilateral, segmental arrangement is evident (Fig. 216). In the two cranial segments, however, unpaired centers occur.

The Skull. -The head skeleton includes three primary components: (i) the brain case; (2) capsular investments of the sense organs; (3) a branchial-arch skeleton, derived from the peculiar arches that enclose the first part of the alimentary tract in all embryos and in adult fishes and tailed amphibia (cf. p. 77). Apart from exceptions in the third group, these elements unite intimately into a composite mammalian skull.

The notochord originally extends into the head as far as the pharyngeal membrane. Not only is the skull built around it, but the accommoda.


217 .

tion of the cerebral hemispheres has made necessary a prechordal development which includes those bones in front of the sella turcica.

The earliest anlage of the skull is a mass of dense mesenchyme, which, at the end of the first month, envelops the cranial end of the notochord and extends cephalad into the nasal region. Laterally, it forms wings which enclose the neural tube. Mesodermal segments do not form in front of the otocysts, so, except in the occipital region, where there are indications of the incorporation of three or four vertebrae, the skull is from the first devoid of segmentation.

.Early in the second month chondrification begins mesially in the future occipital and sphenoidal regions, and extends cephalad and to a slight .


- Interparietal Supraoccipital --Exoccipital Condyle

- Basioccipital 

Fig. 2 18. - Occipital bone of a human fetus of four months. The portions still cartilaginous are shown as a homogeneous background.


Fig. 217. - The chondrocranium of a 14 mm. human embryo (Levi in McMurrich). as, Alisphenoid; bo, basioccipital; bs, basisphenoid; eo, exoccipital; ni, Meckel - s cartilage; os, orbitosphenoid; p, periotic; ps, presphenoid: so, sella turcica; s, supraoccipital.


extent dorsad. At the same time, the internal ears become invested with cartilaginous periotic capsules which eventually unite with the occipital and sphenoidal cartilages (Fig. 217). The chondrocranium, as it is termed, is thus confined chiefly to the base of the skull, whereas the bones of the sides, roof, and the face are of membranous origin. Chondrification also occurs more or less extensively in the branchial arches.

In the period of ossification, which now ensues, it beeomes evident that some bones which are separate in adult lower animals fuse to form compound bones in the human skull. The sphenoid and temporal bones, for example, represent five primitive pairs each. As such components may arise either in membrane or cartilage, the mixed nature of various adult bones is explained.

.A striking feature of the fetal skull is the great relative size of the neural portion. The ratio of cranial to facial volume decreases from 8; i at birth to 2.5:1 in the adult.


2i8 .


Ossification of the Chondrocranium

The Occipital Bone

Ossification begins in the occipital region during the third month (Fig. 222). Four centers a])pear at right angles about the foramen magnum (Fig. 218). From the ventral center arises the basilar (hasioccipital) part of the future bone; from the lateral centers the lateral {cxocci pital) portions which bear the condyles; and from the dorsal, originally paired center, the squamous {supraocci pital) part below the superior nuchal line. The squamous {interparietal) area above that line is an addition of intramembranous origin. These several components do not fuse completely until about the seventh year.

Fig. 219. - Sphenoid bone of a human fetus of nearly four months. Parts still cartilaginous are represented in stipple.

Fig. 220 . - Ethmoid bone of a human fetus of four months.

The Sphenoid Bone

Ten principal centers arise in the cartilage that corresponds to this bone (Fig. 219): (i and 2) in each ala magna {ali sphenoid) - , (3 and 4) in each ala parva {orbitosphenoid ) ; (5 and 6) in the corpus between the alee magnac (basisphenoid) (7 and 8) in each lingula - , (9 and 10) in the corpus between the alee parvae (presphenoid). Intramembranous bone also enters into its composition, forming the orbital and temporal portion of each ala magna and the mesial laminae of each pterygoid Fig. 221. - The left temporal pi'occss (except the hamulus). Fusion of the bone at birth. The portion of various regions is Completed during the first intracartilaginous origin is repre- y0g^j suited in stipple. The Ethmoid Bonc. - The ethmoid cartilage consists of a mesial mass, which extends from the sphenoid to the tip of the nasal process, and of paired masses lateral to the olfactory fossai. The lower part of the mesial mass persists as the cartilaginous nasal septum, but ossification of the upper portion produces the lamina per pendicularis and the crista galli (Fig. 220). The lateral masses ossify at first into the spongy bone of the ethmoidal labyrinths. From this, the definitive honeycomb structure (ethmoidal cells) and the concha; are formed through evaginations of the nasal mucous membrane and the coincident resorption of bone. (Similar invasions of the mucous membrane and dissolution of bone produce the frontal, sphenoidal, and maxillary sinuses: p. 297.) Fibers of the olfactory nerve at first course between the unjoined mesial and lateral masses. Later, cartilaginous, and finally, bony trabeculse surround these bundles of nerve fibers; as the cribriform plates, they . interconnect the three masses.

The Temporal Bone

Several centers of ossification in the periotic capsule unite to form a single center from which the whole cartilage is transformed into the petrous and mastoid portions of the temporal bone (Figs. 221 and 222). The mastoid process is formed after birth by a bulging of the petrous bone; its internal cavities, the mastoid cells. are formed and lined by the evaginated epithelial lining of the middle ear. The squamosal and tympanic portions of the temporal bone are of intramembranous origin, while the styloid process originates from the proximal end of the second, or hyoid branchial arch.

Fig. 222. - The extent of ossification in a fetus of u weeks (after Broman). X 1.5.

Membrane Bones of the Skull

From the preceding account it is evident that, although the bones forming the base of the skull arise chiefly in cartilage, they receive substantial contributions from membrane bones. The remainder of the sides and roof of the skull is wholly of intramembranous origin, each of the parietals forming from a single center, the frontal from paired centers (Fig. 222). At the incomplete angles between the ])arietals and their adjacent bones, union is delayed for some time after birth. These membrane-covered spaces constitute the fontanellcs, or - soft spots - .

The vonier forms from two centers in the connective tissue flanking the lower border of the lamina perpendicularis of the ethmoid. The cartilage of the ethmoid thus invested undergoes resorption. Single centers of ossification in the mesenchyme of the facial region give rise to the nasal, lacrimal, and zygomatic, all pure membrane bones. The maxillary and palate bones are described in the next paragraph.


Cricoid cartilage ( Meckel's cartilage (1) Hyoid cartilage [lesser horn) (u) Hyoid cartilage (greater horn) (uI) Thyroid cartilage (IV -|- V) -Lateral dissection of the head of a human fetus, showing the derivatives of the branchial arches (after Kollmann).


Malleus (I) Incus (I) .

Temporal squama .

Stapes (u) .

Styloid process (u Tympanic ring Stylo-hyoid lig. (u) .

Mandible .

Branchial-Arch Derivatives. - The first branchial arch on each side forks into an upper maxillary and a lower mandibular process (Fig. 64). Cartilage fails to appear in the maxillary processes, due to accelerated development, hence the palate bones and the maxillcr arise directly in membrane (Fig. 222). Each palate bone develops from a single center of ossification. According to recent investigations, two centers contribute to the formation of each maxilla ; one gives rise to the portion bearing the incisor teeth, the other to the remainder of the maxilla.

The entire core of the mandibular process becomes a cartilaginous bar, Meckel - s cartilage, which extends proximally into the tympanic cavity of the ear (Figs. 222 and 223). Alembrane bone, developing distally in the body of the future lower jaw, encloses Meckel - s cartilage and the inferior alveolar nerve, whereas proximally in the ramus the membrane bone merely lies lateral to these structures - hence the position of the adult mandibular foramen. The portion of Meckel - s cartilage invested by bone disappears, while the cartilage proximal to the mandibular foramen becomes in order, the s pheno-mandibular ligament, the malleus, and the incus (p. 310 and Fig. 310).

.Each second branchial arch enters into relation proximally with the periotic capsule. This upper segment of the cartilage becomes the stapes and the styloid process of the temporal bone (Figs. 223 and 310). The succeeding distal portion is transformed into the stylo-hyoid ligament; it connects the stjdoid process with the distal end of the arch, which also undergoes intracartilaginous ossification to form the lesser horn of the hyoid bone.

The cartilage of the third branchial arches ossifies and gives origin to the greater horns of the hyoid bone, while a plate connecting the two arches becomes its body.

The fourth branchial arches differentiate into the cuneiform cartilages and most of the thyroid cartilage.

The fifth branchial arches appear to contribute to the thyroid cartilage and to form the corniculate, arytenoid, and cricoid cartilages.

The Appendicular Skeleton

The appendicular skeleton apparently is derived from the unsegmented somatic mesenchyme, and not from the sclerotomes. In embryos of 9 mm., mesenchymal condensations have formed definite blastemal cores in the primitive limb buds (Figs. 212 and 227). Following this condition, the various bones pass through cartilaginous and osseous stages.

The Upper Extremity. - The clavicle is the first bone of the skeleton to ossify, centers appearing at each end (Fig. 222). Prior to ossification, it is composed of a peculiar tissue which makes it difficult to decide whether the bone is intramembranous or intracartilaginous in origin.

The scapula arises as a single plate with two chief centers of ossification (Fig. 222). An early center forms the body and spine. The other, after birth, gives rise to the rudimentary coraeoid process, which in lower vertebrates extends from the scapula to the sternum. Union between the coracoid process and the body is delayed until about the fifteenth year.

The humerus, radius, and ulna ossify from single primary centers and two or more epiphyseal centers (Figs. 209 and 222).

In the cartilaginous carpus there is a proximal row of three, and a distal row of four elements. Other inconstant cartilages may appear, and subsequently disappear or become incorporated into the carpal bones.

The mctacar pals and phalanges develop from single primary and epiphyseal centers.

The Lower Extremity.- - The cartilaginous plate of the coxal, or hip bone is at first so placed that its long axis is perpendicular to the vertebral column (Fig. 227). Later, it rotates to a position parallel with the vertebral column, and shifts slightly caudad to come into relation with the first three sacral vertebrae (Fig. 222). A retention of the membranous condition in the lower half of each primitive cartilaginous plate accounts for the obturator membrane which closes the foramen of the same name. Three centers of ossification ajjpear, forming the ilium, ischium, and pubis. The three bones do not fuse completely until about puberty.

The general development of the femur, tibia, fibula, tarsus, metatarsus, and phalanges is c|uite similar to that of the corresponding bones of the upper extremity. The patella, like the pisiform of the carpus, is regarded as a sesamoid bone; both develop within tendons.

Anomalies. - Variations in the size, shape, and number of skeletal parts are common. Developmental arrest and over- development are the prime causative factors. Variations in the number of vertebra? (except cervical) are not infrequent. The last cervical and first lumbar vertebra? occasionally bear ribs, due to the continued development of the primitive costal processes. Cleft sternum or cleft xiphoid process represents an incomplete fusion of the sternal bars. Additional fingers or toes (polydactyly) may occur; the cause is obscure. More rarely, there is fusion between two or more digits {syndactyly). Hare lip and cleft palate are described in an earlier chapter (pp. yq; 8q).

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   Developmental Anatomy 1924: 1 The Germ Cells and Fertilization | 2 Cleavage and the Origin of the Germ Layers | 3 Implantation and Fetal Membranes | 4 Age, Body Form and Growth Changes | 5 The Digestive System | 6 The Respiratory System | 7 The Mesenteries and Coelom | 8 The Urogenital System | 9 The Vascular System | 10 The Skeletal System | 11 The Muscular System | 12 The Integumentary System | 13 The Central Nervous System | 14 The Peripheral Nervous System | 15 The Sense Organs | C16 The Study of Chick Embryos | 17 The Study of Pig Embryos | Figures Leslie Arey.jpg


Arey LB. Developmental Anatomy. (1924) W.B. Saunders Company, Philadelphia.

Cite this page: Hill, M.A. (2020, October 30) Embryology Book - Developmental Anatomy 1924-10. Retrieved from

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