Book - Comparative Embryology of the Vertebrates 4-20

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

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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 Development of the Coelomic Cavities

A. Introduction

1. Definitions

The coelomic cavities are the spaces which come to surround the various viscera of the body such as the pericardial cavity around the heart, the pleural cavities surrounding the lungs, and the peritoneal cavity in which lie the stomach, intestines, reproductive organs, etc. These coelomic spaces and recesses arise from a generalized basic condition known as the primitive splanchnocoelic coelom. The primitive splanchnocoelic coelom is the elongated cavity which extends throughout the trunk region beginning just anterior to the heart and continuing posteriorly to the base of the tail. It encloses the developing heart and the developing mesenteron (gut) from the esophageal region posteriorly to the anal region.

2. Origin of the Primitive Splanchnocoelic Coelom

As observed previously (Chapter 10) the elongated mesodermal masses lying along either side of the developing neural tube, notochord, and enteric tube have a tendency to hollow out to form a cavity within. That is, like the neural, gut, and epidermal areas of the late gastrula, the two mesodermal masses tend to assume the form of tubes.

In the case of Amphioxus, each individual somite forms a cavity, the myocoel. These myocoels merge on either side in their ventral halves to form an elongated splanchnocoel below the horizontal septum (see page 506). Later the two splanchnocoels fuse below the developing gut to form the single splanchnocoelic coelom which comes to surround the gut. In the vertebrate group, however, the two elongated splanchnocoels on either side of the developing gut tube and heart form directly in the hypomeric (lateral plate) area of the mesodermal masses without a process of secondary fusion as in Amphioxus. In the upper part of each mesodermal mass, that is in the epimere, and to some extent also in the mesomere (nephrotomic plate) in the vertebrate group as in A mphioxus, there is a tendency for the coelomic spaces to appear in segmental fashion within the primitive somites and within the anterior portion of the mesomere. These individual spaces within the somites are called myocoels, and the spaces which arise in the segmented portion of the nephrotome are called the nephrocoels.

In young shark embryos, such as the 3-4 mm. embryo of Squalus acanthias, and in amphibian embryos of the early post-gastrular period, the myocoelic and nephrocoelic portions of the coelom are continuous dorso-ventrally with the splanchnocoelic coelom (fig. 217G and H). (Actually, during the early stages of coelomic development within the mesodermal masses, in the shark and amphibian embryos, the coelom within the epimere and nephrotomic portions of the mesoderm is continuous antero-posteriorly and it is only after the appearance of the primitive somites and segmentation within the nephrotome that they become discontinuous.) On the other hand, in the embryos of higher vertebrates, the respective myocoels within the somites appear later in development, and in consequence they are always separated from the splanchnocoel. Similarly, the nephrocoelic coelom also arises later and only the separate nephrocoels which develop within the pronephric tubules and certain types of mesonephric tubules make contact with the splanchnocoelic portion of the coelom.

In all vertebrates (see figures 254, 332F-M) the formation of the primitive, generalized coeiomic cavity proper or generalized splanchnocoelic portion of the coelom is formed by the fusion around the developing heart and gut structures of the two elongated splanchnocoels present in the hypomeric portions of the mesodermal masses as described below.

B. Early Divisions of the Primitive Splanchnocoelic Coelom

1. Formation of Primitive Suspensory Structures

The splanchnic walls of the early coeiomic cavities (splanchnocoels) within the two hypomeres become apposed around the structures, lying in the median plane (fig. 254). In the region of the heart, this apposition gives rise to the dorsal and ventral mesocardia and to the epimyocardium of the heart itself (fig. 254A, B) and, in the region of the stomach and intestine, it produces the dorsal and ventral mesenteries of the gut tube and various ligaments, connecting one organ with another. The mesenchyme which arises from the two splanchnic layers also gives origin to the muscles and connective tissues of the gut and its evaginated structures (fig. 31 lA, B). The ventral mesocardium disappears in all vertebrates (Chap. 17). The dorsal mesocardium may persist for a while but eventually disappears entirely or almost entirely (Chap. 17). The dorsal mesentery is present constantly in reptiles and mammals but may be perforated and reduced in the intestinal area in other vertebrate classes, so that little of the dorsal mesentery remains to suspend the intestine in certain cases as, for example, in the shark. The dorsal mesentery above the stomach, the mesogastrium, and also the ventral mesentery in the immediate region between the stomach and liver and between the liver and the ventral body wall persist in all vertebrates. As a rule, however, the ventral mesentery disappears caudal to the liver with the exception of dipnoan and anguilliform fishes and the ganoid fish, Lepisosteus. In these forms the ventral mesentery tends to persist throughout the peritoneal cavity. It follows, therefore, that the two bilaterally developed, splanchnocoelic cavities tend to merge into one cavity or generalized splanchnocoel with a partial retention in certain areas of the splanchnic layers of the two hypomeres which act as suspensory ligamentous structures for the viscera.

2. Formation of the Primitive Transverse Division of the Body and the Primary Pericardial and Peritoneal Divisions of the Coelom

The primitive splanchnocoelic coelom soon becomes divided into the pericardial coelom, surrounding the heart, and the peritoneal or abdominal coelom, surrounding the digestive viscera, by the formation of the lateral mesocardia

Fig. 362. The lateral mesocardia form the initial division of the embryonic coelom (A-1 and A-2) represent idealized sections through the vertebrate embryonic body in £ plane bet\veen the caudal limits of the sinus venosus and the anterior extremity of th( potential liver region of the embryo. (A-1) Diagram of the initial stage of separatior of the pericardial and peritoneal coelomic cavities in many vertebrates. Two dorsal anc two ventral recesses or passageways above and below the lateral mesocardia and latera horns of the sinus venosus are evident. These passageways communicate with the peri cardial and peritoneal divisions of the primitive coelom. (A-2) Separation of primitive

and the primitive septum transversum which develop in relation to the converging veins of the sinus venosus and the ventro-cephalic growth of the liver rudiment. In other words, a ventral partition is established across the primitive splanchnocoelic coelom in a plane which separates the caudal end of the heart (i.e., sinus venosus) from the anterior limits of the liver. This primitive transverse partition partially separates the primitive splanchnocoelic coelom into two main divisions:

( 1 ) a cephalic compartment, the pericardial cavity, around the heart and coelom into anterior pericardial and posterior peritoneal areas in early human embryo. The precocious development of the caudal wall of the parietal pericardium obliterates the ventral recesses shown in A-1 previous to septum transversum formation and the outgrowth of the liver rudiment. Communication between pericardial and peritoneal coelomic divisions is possible only through the dorsal parietal recesses (dorsal pericardioperitoneal canals). (B) Schematic diagram representing the initial division by the lateral mesocardia of the primitive coelomic cavity into anterior pericardial and posterior peritoneal divisions in an embryo of Squalus acanthias 10 mm. long. The liver outgrowth has been extended forward slightly for diagrammatic purposes. (C) Initial division, by the lateral mesocardia, of the primitive coelom in the 72 hr. chick embryo. Due to the depressed condition of the anterior end of the body much of the heart appears in the section below the sinus venosus and lateral mesocardia. However, if the embryo were straightened and the atrium, etc., of the heart pushed forward, the structural conditions would appear much the same as in B. The dorsal parietal recesses appear on either side of the esophagus. (D) Semidiagrammatic section through caudal end of sinus venosus of 22 mm. shark embryo. The dorsal closing folds are developing on either side of the esophagus, thus closing the dorsal recesses. The liver rudiment is expanding within the substance of the ventral mesentery caudal to the heart to form the liver’Septiirn transversum complex. The latter structure obliterates the ventral recesses below the lateral mesocardia. (E) Diagrammatic representation of the forward and ventral growth of the developing liver within the substance of the ventral mesentery to form the liverseptum transversum complex. (See fig. 363D.) Observe: ventral parietal recesses are obliterated by the forward growth of this complex of tissues. The arrow denotes the passageway from the pericardial coelom into the peritoneal coelom through the dorsal parietal recesses (dorsal pericardioperitoneal canals). (F) Early stage in development of human heart and septum transversum showing ingrowth of somatopleural mesoderm between the previously formed caudal wall of the parietal pericardial membrane (see A-2) and the entoderm of the anterior intestinal portal. (Redrawn from Davis, 1927, Carnegie Inst. Public. 380, Cont. to Embryology, 107.) (G) Later stage of human

heart development. Mesodermal partition (septum transversum) is present as a thickened mass of tissue below the developing sinus venosus and between the caudal wall of the parietal pericardium and the gut entoderm. (Redrawn from Davis, see fig. 362F, for reference.) (H) Lateral dissection of fifth week human embryo to show ingrowth of liver tissue into thickened septum transversum. (Redrawn from Patten, 1946, Human Embryology, Blakiston, Philadelphia.) Arrow denotes passageway (dorsal parietal recess; pericardioperitoneal canal; pleural canal) between pericardial and peritoneal coelomic cavities. (I-l) Sagittal section through 15 mm. pig embryo showing thickened anterior face of liver. This thickened anterior face of the liver later separates from the liver as the primary septum transversum (peritoneo-pericardial membrane). (1-2) Higher powered drawing to show condition of anterior face of liver shown in fig. 362, I-l. (J) Transverse section through thorax and pulmonary area of the body of a bird to show position of dorsal pulmonary diaphragm. (Redrawn from Goodrich, 1930, Studies on the Structure and Development of Vertebrates, Macmillan Co., Limited, London.) Observe position of liver lobes in relation to the heart. Compare with fig. 294, G-4 & G-5.

Fig. 362 — (Continued)

See legend on p. 860 .

(2) a larger caudal compartment, the peritoneal cavity, around the digestive viscera and urogenital structures.

This primary division of the early coelomic cavity is accomplished by the formation of:

1 ) The lateral mesocardia, and

2) the primary (primitive) septum transversum.

The two lateral mesocardia are formed previous to the development of the primitive septum transversum. Eventually the lateral mesocardia fuse in part to the dorsal edge of the transverse septum and become a part of it. The lateral mesocardia thus, in reality, represent the initial stage in the division of the general coelomic cavity. In consequence we shall consider the lateral mesocardia as important structures which enter into the formation of the primary transverse division of the embryonic body, but they should not be confused with the primitive septum transversum in a strict sense.

a. Lateral Mesocardia

The lateral mesocardia (fig. 362A-1, A-2) are formed as follows:

A lateral bulging or growth from the splanchnopleure at the caudal limits of the developing sinus venosus extends dorso-laterad on each side to meet a somewhat similar though smaller growth mediad of the somatopleural mesoderm. These growths form a bridge on each side across the coelomic cavity, extending dorso-laterad from the posterior lateral edges of the ventrally situated sinus venosus to the somatic wall. The area of union of this bridge on either side with the lateral body wall is the lateral mesocardium. The lateral mesocardia, in other words, represent the areas of juncture between the lateral body walls and the lateral extensions of the sinus venosus. The common cardinal veins or ducts of Cuvier join these right and left lateral extensions or horns of the sinus venosus in the substance of the lateral mesocardia. Anterior to the lateral mesocardia is the pericardial coelom, while posterior to them is the peritoneal coelom. The two passageways dorsal to the lateral mesocardia, on either side, are called the dorsal parietal recesses of His, while those ventral to the lateral mesocardia and on either side of the ventral mesentery and developing liver constitute the ventral parietal recesses of His (fig. 362A).

b. Formation of the Liver-Septum Tramversum Complex

1) Formation of Liver-Septum Complex through Modification of the Ventral Mesentery by Liver Outgrowth. As the liver rudiment in the shark, chick, pig, etc., grows ventrally and forward between the two splanchnopleural layers of the ventral mesentery, it expands the ventral mesentery laterally as the liver substance forms within the mesenchyme between the two splanchnic layers. The expanding liver substance eventually reaches the ventral and lateral

Fig. 363 (A-1, 2, 3). Diagrams showing the invasion of the peritoneal coelom around the liver and relations of septum transversum and diaphragm to the liver. (A-1) The peritoneal invasion separates the liver substance away from the lateral body wall and also from the anterior face of the liver itself. The separated, thickened, anterior face of the liver (see fig. 362, I-l and 1-2) forms the primary septum transversum (peritoneopericardial membrane). (A-2) The relation of the liver and other viscera to the secondary septum transversum formed by the addition of the dorsal closing folds (see fig. 362D) to the primary septum transversum. (A-3) This is a diagrammatic representation of conditions shown in B. Observe position of various ligaments associated with the liver. (B) Sagittal section through opossum embryo presenting relation of the liver to diaphragm. The ventral part of the diaphragm is the remodeled primary septum transversum. Observe that the inferior vena cava perforates the diaphragm. The area of attachment of the liver to the diaphragm is the coronary ligament, (The preparation from which this drawing was made was loaned to the author by Dr. J. A. McClain.) (C) Pericardioperitoneal opening below the esophagus in the shark, Squalus acanthias. (See also fig. 362D.) (D) Schematic diagram, dorsal view, of initial stage of devel oping pleural cavities in the mammal showing the anterior and posterior lateral body folds. The anterior lateral body fold gives origin to the pulmonary ridge or rudiment of the pleuropericardial membrane and the posterior lateral body fold forms most of the pleuroperitoneal membrane. Cf. fig. 362E. (E-H) Schematic diagrams showing later

stages in separation of pleural cavities in the mammal, viewed from the dorsal aspect. Observe that the pleuroperitoneal membrane is formed from two rudiments, viz., the posterior lateral body fold and a very small splanchnopleuric contribution (fig. 363F).

Fig. 363 — (Continued)

body wall, where it fuses with the somatopleure from the body wall. Since the lateral expansion of the developing liver is more rapid than its forward growth, the anterior face of the liver gradually becomes flattened in the area just below (ventral to) the lateral mesocardia and immediately posterior to the sinus venosus of the heart. The mesenteric tissue, covering the anterior face of the liver, then fuses with the more dorsally located, lateral mesocardia. A transverse division across the body is completed in this manner below the lateral mesocardia, and the ventral parietal recesses in consequence are closed. Passage from the pericardial cavity to the peritoneal (abdominal) cavity is now possible only by way of the pericardioperitoneal canals (dorsal parietal recesses) (fig. 362E).

Although liver-rudiment development in the embryo of the frog and in the embryos of other amphibians is precocious the essential procedure in the formation of the primitive liver-septum transversum complex is similar to that described above.

2) Formation of the Liver-Septum Complex in the Human Embryo. In the developing human embryo, medial growths on either side from the somatopleural mesoderm occur in the region caudoventral to the forming sinus venosus, and below the developing gut tube. In this way ,a primitive transverse septum is formed below the lateral mesocardia and between the entoderm of the gut and the caudal wall of the parietal pericardium (fig. 362F, G). This septum fuses with the lateral mesocardia and caudal wall of the parietal pericardium. However, when the evaginating liver rudiment grows ventrad and forward into the splanchnopleural tissue below the gut, it ultimately appropriates the previously formed transverse septum as its anterior aspect. Consequently, the general result of the two methods is the same, namely, the transverse septum in its earlier stages of development appears as the thickened anterior face of the liver associated with the lateral mesocardia (figs. 261 A; 362H, I).

c. Formation of the Primary Septum Transversum

After the liver-septum transversum complex has been established and the potential ventral parietal recesses are closed by either of the two methods described above, the next stage in the development of the primitive septum transversum is correlated with the forward expansion of the peritoneal coelom around the sides and anterior face of the liver. In doing so, the peritoneal coelom on either side of the liver extends anteriad and mesiad and thus becomes involved in a secondary separation of the liver from the lateral and ventral body wall and also from the anterior face of the liver itself which becomes the primary septum transversum (fig. 363 A, B). A separation does not occur in the area traversed by the veins passing from the liver to the sinus venosus or slightly dorsal to this area. Here the liver remains attached directly to the septum transversum and is suspended literally from it. This attaching tissue forms the coronary ligament of the liver. The ingrowth of the two coelomic areas on either side of and ventral to the liver, by apposition of the coelomic epithelium in the median plane, forms a secondary ventral mesentery of the liver. This secondary ventral mesentery or falciform ligament ties the liver to the mid-ventral area of the body wall and to the septum transversum. {Note: The terms primary septum transversum and peritoneopericardial membrane are synonymous.)

C. Coelomic Changes in Fishes, Amphibians, Reptiles, and Birds

1. In Fishes

In the adult shark, and fishes in general, the fully developed adult form of the septum transversum forms a complete partition between the pericardial cavity and the peritoneal cavity. In fishes the pericardial cavity in the adult fish, as in the embryo, extends laterally and ventrally to the body wall in a fashion similar to that of the peritoneal cavity. Also, the heart continues to lie posterioventrally to the pharyngeal region in a manner very similar to that of the basic, embryonic body plan (fig. 294G-I).

In the formation of the adult, piscine, septum transversum from the primary transverse septum two membranous partitions are developed which close the dorsal parietal recesses or the openings above the lateral mesocardia. These partitions are called the dorsal closing folds and they arise as follows:

The splanchnopleural tissue on either side of the foregut, just anterior to the stomach rudiment and above the primitive septum transversum, forms a thin fold of tissue. This fold grows laterad and ventrad and fuses ultimately with the lateral mesocardium and the somatopleuric tissue, which overlies the common cardinal vein, as this vein travels caudo-ventrally along the body wall to reach the lateral mesocardium and the sinus venosus. As a result of this splanchnopleuric and somatopleuric fusion of tissues with the dorsal edge of the primary septum transversum a dorsal closing fold is formed on either side of the esophagus, and the two dorsal parietal recesses are obliterated, separating completely the pericardial cavity from the peritoneal cavity (fig. 362D). However, a small pericardioperitoneal opening may be left below the esophagus in the shark.

The secondary septum transversum thus formed is a thickened transverse partition, composed of two walls, an anterior pericardial wall and a posterior peritoneal wall, with a loose tissue layer between these two coelomic membranes. The liver is suspended from the peritoneal or caudal aspect of the septum transversum in the region of the coronary ligament, while the posterior end of the sinus venosus is apposed against the anterior or pericardial face of the transverse septum. The common cardinal and other converging veins of the heart utilize the substance of the septum transversum as a support on their way to the sinus venosus. The hepatic veins (the right and left, embryonic vitelline veins) pass through the coronary ligament on their journey to the sinus venosus.

2. In Amphibians, Reptiles, and Birds

The conversion of the primary septum transversum in amphibians, reptiles, and birds into the secondary or adult septum transversum occurs essentially as described above. A dorsal closing fold, obliterating the dorsal parietal recess on either side of the gut, is developed, although, in reptiles and birds, the inward growth and contribution of somatopleuric tissue overlying the common cardinal ridge is more important than in fishes in effecting this closure.

However, one must keep in mind an important fact, namely, that, in amphibia, reptiles and birds, there is an extensive caudal migration of the heart, septum transversum, and liver complex from their original cephalic position just posterior to the pharyngeal area. This caudal migration produces a condition in which the primary septum transversum and the dorsal membranes, formed by the dorsal closing folds, are inclined to a great degree, with the ventral end of the primary septum transversum considerably more posterior in position than the dorsal edge of the dorsal membranes. Consequently, a secondary recess or pocket is formed on either side anterior and dorsal to the septum transversum. This secondary recess occurs on either side of the gut, and, into each of these recesses, a lung extends in many reptiles and in those amphibia which possess lungs. In this pocket also lie certain of the air sacs of birds. Thus, the general cavity back of the pericardioperitoneal membrane or secondary septum transversum (i.e., the primary septum transversum plus the two dorsal membranes, formed by the dorsal closing folds) is known as the pleuroperitoneal cavity in amphibia and many reptiles. In birds (see below), the respiratory part of the lung becomes enclosed dorsally near the vertebrae within a separate pleural cavity, separated from the peritoneal cavity by the dorsal diaphragm (fig. 362J). The thin air sacs of the bird’s lung (Chap. 14) project from the lung through the dorsal diaphragm into the peritoneal cavity and also into certain of the bones. In the turtle group, among the reptiles, a dorsal diaphragm is developed below each lung, segregating the lungs partly within dorsal cavities, thus simulating the bird condition.

D. Formation of the Coelomic Cavities in Mammals

In the mammalia, a pronounced caudal migration of the heart, liver, and developing diaphragm occurs. Also, as in birds, a further morphogenetic feature is present which results in the development of a pleural cavity for each lung in addition to the peritoneal and pericardial cavities present in fishes, amphibians, and reptiles. Thus it is that the development of two partitioning membranes on either side of the gut tube, the pleuropericardial membranes, which correspond to the dorsal closing membranes mentioned above, together with two additional membranes, the pleuroperitoneal membranes, are necessary to effect the division of the primitive splanchnocoelic coelom into the four main coelomic cavities in the Mammalia.

1. Formation of the Pleuropericardial Membrane

It so happens that the anterior cardinal vein develops slightly in advance of the posterior cardinal vein. As a result the common cardinal vein, which develops from the caudal end of the primitive anterior cardinal vein, travels along the lateral body wall in an inclined plane to reach the area of the lateral mesocardium and sinus venosus of the heart. This inclined pathway of the common cardinal vein is characteristic of the vertebrate embryo. As the common cardinal vein increases in size, a lateral ridge or elongated bulge is formed along the lateral body wall. This ridge projects inward into the coelomic cavity and inclines caudo-ventrally to reach the dorsal edge of the area of the primitive septum transversum (fig. 363D).

In the mammals, the mesonephric folds (ridges), in which the mesonephric kidneys develop, are large and project downward into the coelomic cavity. The anterior ends of the mesonephric ridges continue along the lateral body wall on either side and follow an inclined plane antero-ventrally to the dorsal edge of the primitive septum transversum (fig. 363D). Two lateral body folds or ridges, which incline toward and fuse with the dorsal edge of the primitive septum transversum, are produced in this manner on either side. These folds are an anterior lateral body fold or ridge, overlying the common cardinal vein, and a posterior lateral body fold, which represents the antero-ventral continuation of the mesonephric ridge as it inclines ventrally to join the lateral edge of the primitive septum transversum (fig. 363D). A V-shaped pocket is formed between these two ridges. This pocket represents the primitive pleural cavity or pocket. The apex of this V-shaped pocket unites with the primitive septum transversum. As the lung buds grow out posteriorly below the foregut, each projects into a pleural pocket (fig. 363F).

The formation of the pleuropericardial membrane is effected by an ingrowth of tissue along the edge of the anterior, lateral body fold, the fold that overlies the common cardinal vein. This ingrowing tissue forms a secondary ridge, known as the pulmonary ridge, which continues to grow mesad below the developing lung until it reaches the splanchnopleure of the esophagus with which it fuses. A pleuropericardial membrane, in this way, is established which separates the pericardial cavity below from the pleural cavity above (fig. 363E-G). The pleuropericardial membranes probably arc homologous with the dorsal closing folds of the secondary septum transversum of the vertebrates below the mammals.

2. Development of the Pleuroperitoneal Membrane

As mentioned previously, the cephalic end of the mesonephric ridge projects forward and ventrad along the lateral body wall to unite with the primitive septum transversum to form the posterior, lateral body fold. The medial growth of this posterior, lateral body fold and ultimate fusion with a small splanchnopleural outgrowth, the splanchnopleural fold, forms a second partitioning membrane, the pleuroperitoneal membrane, which separates the pleural cavity from the general peritoneal cavity (fig. 363E-H). Contributions of the somatic mesoderm to the lateral body-fold tissue are significant in the formation of the pleuroperitoneal membrane. It is to be noted that the primitive pleural cavities of the mammalian embryo are small and dorsally placed, one on either side of the gut and dorsal to the pericardial cavity. Their later expansion is described below. To summarize the partitioning process of the primitive coelom in mammals, we find that the following membranes are formed:

( 1 ) the primary septum transversum,

(2) the two dorsal closing folds or pleuropericardial membranes, and

(3) two pleuroperitoneal membranes.

Fig. 364 (A). Transverse section of the thoracic area of opossum embryo showing the separation of the parietal pericardium from the lateral body walls by expanding pleural sacs. (The preparation from which this drawing was made was loaned to the author by Dr. J. A. McClain.) (B-1) Transverse section through lung buds and pleural

E. Development of Independent Pericardial Walls

1. The Arrangement of the Parietal Pericardial Wall in Fishes

The parietal pericardium of the fish embryo is fused with the lateral body wall. The caudal area of the sinus venosus is associated intimately with the anterior wall of the septum transversum. This condition is a primary one in all vertebrate embryos. It is retained in the adult fish.

2. Formation of an Independent Parietal Pericardial Wall in the Chick

In the chick, two main processes occur in development which separate the septum transversum from the liver, and also the parietal pericardial membrane from the lateral body walls. These processes are:

(a) The peritoneal cavity on either side of the liver grows forward and separates the cardiac or anterior face of the liver from the posterior face of the septum transversum, with the exception of the area where the veins from the hepatic region perforate the septum. This process frees the septum transversum from the liver surface and permits it to function as a part of the pericardial sac as indicated in figure 294G-4; G-5.

(b) The extending peritoneal coelom not only separates the liver from the posterior face of the septum transversum, but it continues anteriad followed by the liver lobes along the ventral and lateral aspects of the body wall and splits the membranous pericardium away from the lateral body wall. Ventrally, a median septum unites the pericardium with the body wall (fig. 362J).

3. Formation of the Independent Parietal Pericardial Wall in Amphibians and Reptiles

A somewhat similar process to that described for the chick obtains in reptiles and, to a modified extent, in amphibia.

Fig. 364 — Continued

cavities of a 10 mm. pig embryo showing position of the primitive mediastinum. (B-2) Later mediastinal area development portraying adult position (black area) of the mediastinum. (Based on the cat.) Observe that fig. 364 (A) is an intermediate condition between figs. 364 (B-1) and 364 (B-2). (C) Probable origin of parts of the mammalian diaphragm. (D) The caudal migration of the septum transversum and developing diaphragm during development. 2-position = embryo of 2 mm.; 24-position = 24 mm. embryo. (Redrawn from F. P. Mall, 1910, Chap. 13, Vol. 1, Manual of Human Embryology, Lippincott, Philadelphia.) (E-H) Development of the mesenteries and omental bursa or lesser peritoneal cavity in the human. The cross-lined areas in H show areas of the mesentery which fuses with the body wall. The arrows in F-H denote development of the lesser peritoneal cavity.

4. Separation of the Parietal Pericardial Wall in Mammals

On the other hand, in the mammals, it is the pleural cavities, i.e., the pleural divisions of the splanchnocoelic coelom, which extend ventrally around the heart and thus separate the parietal pericardium from the thoracic body wall (fig. 364A and B) . Posteriorly, they separate the pericardium from the anterior face of the developing diaphragm (fig. 363B). The secondary condition of the mediastinum thus is established which extends dorsoventrally between the two pleural sacs (fig. 364B-2). It is to be observed that the medial walls of the pleural sacs fuse with the lateral walls of the pericardium by means of the connective tissue which forms between these two layers.

F. The Mammalian Diaphragm

The mammalian diaphragm is a musculotendinous structure, innervated by the phrenic nerve and developed from tissues around the gut, primary septum transversum, the two pleuroperitoneal membranes, and possibly also by contributions from the body wall. Study figure 364C. The exact origin of the voluntary musculature of the diaphragm is in doubt, but it is assumed to come from the cervical myotomes in the region of origin of the phrenic nerve, together with some invasion of muscle substance from the lateral body wall posterior to the cervical area. Successive caudal positions of the septum transversum and developing diaphragm, assumed during its recession in the body, are shown in figure 364D.

G. The Pulmonary Diaphragm or Aponeurosis of the Chick

The pulmonary diaphragm in the chick is a composite structure formed of two membranes which develop in a horizontal position in the dorsal region of the thoracic area below the lungs. Each of these two membranes fuses with the median mesentery and the lateral body wall and thus forms a partition separating the pleural cavities above from the peritoneal cavity below (fig. 362J). The development of this partitioning membrane is as follows:

In the four- to five-day chick as the lung buds grow out dorso-posteriad each lung bud pushes into a mass of mesenchyme which is continuous from the splanchnopleure around the esophagus to the dorsal region of the liver.

This connecting bridge of mesenchyme is the pleuro-peritoneal membrane and it extends from the region of the esophagus across the lower part of the lung bud tissue to the liver lobe on each side. The mesenchymal connection of this membrane with the liver then spreads laterally to unite with the lateral body wall. As a result, the pleural cavity above is shut off from the peritoneal cavity below. A continual growth dorsoposteriad of the pleuro-peritoneal membrane, and subsequent fusion with the dorsal body wall tissues, separates the pleural cavity completely from the peritoneal cavity. However, certain canals remain in this membrane for the passage of the air sacs (see Chapter 14) of the lungs. Striated musculature from the lateral body wall grows into the pleuro-peritoneal membrane on either side and converts it into a muscular structure. These two muscular partitions thus form the pulmonary diaphragm.

H. The Omental Bursa

In all gnathostomous vertebrates, the mesogastrium is prone to form a primitive pocket, associated with the rotation of the stomach to the right. This pocket is quite prevalent in most gnathostomous embryos from the elasmobranch fishes to the mammals and is known as the primitive omental bursa. In mammals, the omental bursa is highly developed, and it gives rise to the lesser peritoneal cavity, retaining its connection with the greater peritoneal cavity by means of the foramen of Winslow. The lesser peritoneal cavity in the cat is extensive, filling the entire inside of the omental sac. In the human, however, the distal part of the lesser peritoneal cavity is reduced by the fusion of the omental layers. Though a rudimentary omental bursa is formed in the early embryonic condition of elasmobranch fishes (sharks), it soon disappears, so that, in the adult fish, the omental bursa is nonexistent. Figure 364E~H presents various stages in the development of the omental bursa in the human embryo.

I. The Formation of Various Ligaments in the Stomach-Liver Region

Ligaments are those specializations of the peritoneal tissue which unite various organs with each other or with the body wall.

1. The Gastro-hepatic and Hepato-duodenal Ligaments. These structures are derivatives of the ventral mesentery between the stomach-duodenal area and the liver. The gastro-hepatic ligament ties the stomach and liver together while the hepato-duodenal ligament unites the duodenum with the liver.

2. The Coronary Ligament of the Liver. This is the tissue which unites the liver with the caudal face of the septum transversum and in mammals with the later developed diaphragm. Its development is described on page 866.

3. The Falciform Ligament of the Liver. This unites the liver in the median plane to the ventral body wall and to the septum transversum or diaphragm.

4. The Gastro-splenic Ligament suspends the spleen from the stomach and it represents a modification of the mesogastrium (see Chapter 17).

(Note: Ligamentous structures associated with the reproductive organs are described in Chapter 18.)


Goodrich, E. S. 1930. Chap. XU in Studies on the Structure and Development of Vertebrates. Macmillan and Co., London.

Mall, F. P. 1910. Chap. 13, Vol. I, Manual of Human Embryology, Lippincott, Philadelphia.