Book - Comparative Embryology of the Vertebrates 4-17

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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 Circulatory System

A. Introduction

1. Definition

Living matter in its active state depends for its existence upon the beneficent flow of fluid materials through its substance. This passage of materials consists of two phases:

( 1 ) the inflow of fluid, containing food materials and oxygen, and

(2) the outflow of fluid, laden with waste products.

In the vertebrate group as a whole, the inflow of materials to the body substance occurs through the epithelial membranes of the digestive, integumentary, and respiratory systems, while the outflow of materials is effected through the epithelial membranes of the excretory, respiratory, and skin surfaces. The passage of materials through the substance of the body lying between these two sets of epithelial membranes is made possible by (a) the blood and (b) a system of blood-conveying tubes or vessels. These structures form the circulatory system.

2. Major Subdivisions of the Circulatory System

The circulatory system is composed of two major subdivisions:

  1. the arteriovenous system, composed of the heart, arteries, and veins together with the blood vessels and capillaries of smaller dimensions intervening between the arteries and veins, and
  2. the lymphatic system, made up of lymph sacs, and lymphatic vessels together with specialized organs such as the spleen, tonsils, thymus gland, and lymph nodes. In larval and adult amphibia pulsating lymph hearts are a part of the lymphatic system. Lymph hearts are present also in the tail region of the chick embryo.

The lymphatic vessels parallel the vessels of the arteriovenous system, and one of their main functions appears to be to drain fluid from the small spaces within tissues as well as larger spaces, such as the various divisions of the coelomic cavity.

The blood within the arteriovenous system is composed of a fluid substance or plasma together with red blood corpuscles or erythrocytes, white blood cells of various types, and blood platelets. The latter are small protoplasmic bodies which may represent cytoplasmic fragments of the giant, bone-marrow cells or megakaryocytes. The blood within the lymphatic system is composed of a vehicle the lymph fluid, similar to the plasma of the arteriovenous blood system, together with various white blood corpuscles.

B. Development of the Basic Features of the Arteriovenous System

1, The Basic Plan of the Arteriovenous System

The primitive circulatory system is constructed of three main parts:

( 1 ) two sets of simple capillary tubes, bilaterally developed on either side of the median line (fig. 332),

(2) a local modification of these tubes which forms the rudimentary heart, and

(3) blood cells and fluid contained within the tubes.

2. Development of the Primitive Heart and Blood Vessels Associated with the Primitive Gut

The primitive vascular tubes or capillaries form below the anterior region of the developing metenteron or gut tube in relation to the yolk sac or yolkcontaining segment of the gut. Two sets of identical tubes begin to form, one set on either side of the median plane of the embryo (fig. 3 32 A and B). Simultaneous with the formation of these primitive, subintestinal blood capillaries, the splanchnic layers of the two hypomeric portions of the mesodermal tubes grow mesiad to cup around the blood capillaries in the area just posterior to the forming pharyngeal area of the gut tube (figs. 234; 236D, E; 332F-M). This encirclement of the primitive blood capillaries by the splanchnic layers of the hypomeric mesoderm produces the rudimentary tubular heart, composed within of two fused subintestinal capillaries and without of modified fused portions of the hypomeric mesoderm. The modified portions of the hypomeric mesoderm form the epimyocardial rudiment of the heart, while the fused capillaries within establish the rudimentary endocardium (fig. 332F-M).

Proceeding anteriad from the area of primitive tubular heart, the blood capillaries establish the primitive ventral aortae (fig. 332A).

From the primitive ventral aortae, the two capillaries move forward toward the anterior end of the foregut where they diverge and pass dorsally, one on either side of the foregut, as the first or mandibular pair of aortal arches. In the dorsal area of the foregut the two primitive aortal arches pass inward toward the median plane and each aortal arch joins a primitive capillary which runs antero-posteriorly along the upper aspect of the developing gut tube. These two supraintestinal blood vessels are the rudiments of the future dorsal aorta and they are known as the dorsal aortae. They lie above the primitive gut and below the notochord. In the region where the mandibular pair of aortal arches joins the dorsal aortae, each primitive dorsal aorta sends a capillary sprout toward the developing eye region and the brain. This capillary forms the rudiment of the anterior end of the internal carotid artery. About the midregion of the developing midgut, each of the dorsal aortae sends off a lateral branch which connects with a series of capillaries in the yolk or yolk-sac area of the deveoping midgut. The vessels which diverge from the dorsal aorta to the yolk-sac region form the rudiments of the two vitelline arteries. The capillary network in the yolk region or yolk-sac area of the midgut in turn connect with the two subintestinal capillaries, previously mentioned, which enter the forming heart. The two latter blood vessels constitute the vitelline veins (fig. 332B). Meanwhile, successive pairs of aortal arches are formed posterior to the first pair, connecting the ventral aortae with the dorsal aortae (fig. 332D). These aortal arches pass through the substance of the visceral arches, as mentioned in Chapters 14 and 15.

3. Formation of the Primitive Blood Vessels Associated WITH the Mesodermal and Neural Areas

The system of blood vessels described above (fig. 232A) is developed in relation to the primitive gut tube. Very shortly, however, another system of vessels is established dorso-laterally to the mesodermal tubes. This second system of blood capillaries forms the beginning of the cardinal system (fig. 232B). The cardinal system is composed of two anterior cardinal veins which begin as a series of small capillaries on either side over the forming brain; from whence these veins proceed backward, one on either side over the branchial mesoderm, and lateral to the forming somites. These vessels eventually proceed latero-ventrad in their development along the outer lateral aspect of the somatopleural mesoderm to the caudal regions of the forming heart, where they turn ventrad along the outer aspect of the somatopleural layer of the hypomere. In the region where the anterior cardinal veins turn ventrad toward the heart region, each anterior cardinal vein is joined by a posterior cardinal vein. The latter proceeds forward from the posterior end of the developing embryo, lying along the outer aspect of the nephrotomic portion of the hypomere below the primitive epidermal tube (fig. 332B). The union of the anterior and posterior cardinal veins on either side forms the common cardinal vein. The latter travels postero-ventrally along the outer aspect of the somatopleure until it reaches the upper limits of the caudal region or sinus venosus of the developing heart. In this area, the splanchnopleural layer (epimyocardium) and the endocardial layer of the developing sinus venosus, bulge laterad to fuse with the somatopleural layer of the hypomere. This area of contact between the epimyocardial layer of the sinus venosus and somatopleural mesoderm produces a bridge across the coelomic space. The two posterior, dorso-lateral regions of the sinus venosus thus extend dorso-laterad on either side across the coelomic space to join the somatopleure. Each common cardinal vein perforates through the somatopleure in this area and empties into the sinus venosus at a point lateral to the entry of the two vitelline veins (fig. 332C). This bridge established across the coelomic cavity from the somatopleure of the body wall to the splanchnopleure of the heart forms a lateral mesocardium on either side. The two lateral mesocardia

Fig. 332. Early development of primitive vascular system including tubular heart. (The diagrams included in this figure should be studied together with descriptions in Chapter 10 relative to tubulation of the major organ-forming areas of the early embryo.) (A) Diagram of the early bilaterally developed vascular tubes (capillaries) which form in relation to the primitive gut tube. This system of capillaries constitutes the first or early vitelline system of developing circulatory structures. (B) The cardinal or primary venous system is added to the primitive vitelline system. (C) The area of union between the early vitelline and cardinal systems at the caudal end of the heart. (D) The basic (fundamental) condition of the vascular system. (E) Two diagrams showing the union of the vitelline and cardinal systems distally between the somites and near the nerve cord. The three vascular tubules to the left in this drawing show an early relationship of the intersegmental arteries and veins, and the drawing of the three vascular tubules to the right depict a later stage of this developmental relationship. (F-M) Stages in the development of the early tubular heart in shark, frog, and chick embryos. As the mammal is similar to the chick it is not included. (F~H) Early development of the heart in Squalus acanthias. (F) The lower, mesial edges of the hypomeric mesoderm begins to cup around the primitive subintestinal capillaries. (G) Later stage. (H) A transverse section through the heart which is now in the form of a straight tube comparable to that shown in Fig. 3 39 A. (I-K) Early stages in the development of the frog heart. Observe that the ventral areas of the two hypomeres become confluent and later form a trough-like cup around the forming subintestinal capillaries below the foregut. (Redrawn from Kellicott, 1913. Outlines of Chordate Development, Henry Holt, N. Y.) (L-M)

Early development of the chick heart. (L) At about 26 hrs. of incubation. (M) About 30 hrs. of incubation.

Fig. 332. (See facing page for legend.)

represent the initial stages in the development of the various coelomic divisions of the primitive coelomic space (Chap. 20).

As the cardinal and intestinal systems of the primitive vascular system become joined together centrally via the common cardinal veins, the two systems become joined peripherally by means of a series of intersegmental blood vessels. The latter arise from the dorsal aortae and travel dorsally between the somites and myotomes to the central nerve tube (fig. 232E). In the nerve-tube area, the primitive intersegmental arteries become continuous with the rudiments of the intersegmental veins which course laterad to join the anterior and posterior cardinal veins. When the above vascular channels are well established, another set of veins is formed between the somatopleural mesoderm of the hypomere and the developing integument (figs. 332D; 336C, D). The last veins course along the lateral body wall, arising in the pelvic area and emptying into the sinus venosus of the heart. In fishes and amphibia, these veins are called lateral veins, but in reptiles, birds, and mammals, they are denominated the allantoic or umbilical veins as they drain principally the allantoic area of the embryo.

4. Regions of the Primitive Vascular System

The primitive morphological plan of the vascular system, as outlined above, is a basic condition strikingly comparable in all vertebrate embryos. In view of the later changes of this fundamental vascular plan necessitated by the adaptation of the vascular system to the environmental conditions existing within the various habitats of the adult, it is well to demarcate, for the purposes of later discussion, certain definite regions of the primitive arteriovenous system. These regions are (fig. 332D):

(1) the converging veins of the heart, composed of the lateral, common cardinal, anterior and posterior cardinal, and vitelline veins,

(2) the primitive heart, made up of the primitive sinus venosus, atrium, ventricle, and bulbus cordis,

(3) the branchial area, composed of the ventral aortae, aortal arches, and adjacent dorsal aortae, and,

(4) the dorsal aortae (later aorta) and efferent branches.

C. Histogenesis of the Circulatory System

1. The Heart

Consult Chap. 16.

2. Formation of the Primitive Vascular Channels and Capillaries

Two principal theories have emerged to account for the origin of the primitive blood vessels in the embryo. These theories are the angioblast theory and the local origin theory.

The angioblast theory rests upon the assumption that a special vascular tissue, called the angioblast by Wilhelm His, develops in the area of the yolk sac. This angioblast tissue, according to the angioblast theory, forms a vascular rudiment within which the endothelium, or flattened epithelial cells peculiar to blood capillaries, is developed. This endothelium produces the primitive capillaries of the yolk area, and, further, it grows into the developing embryo where it forms the endothelium of the entire intra-embryonic vascular system. That is, the angioblast in the yolk area provides the source from which arises the endothelial lining of all the primitive blood vessels of the embryo and also of all later endothelium of later blood vessels. The endothelium of all blood vessels thus traces its ancestry back to the yolk-sac angioblast.

The local origin theory may be divided into two schools of thought. One school espouses the idea that “mesenchyme may, in practically any region of the body, transform into vascular tissue” (McClure, ’21, p. 221). Accordingly, primitive blood capillaries arise in loco from mesenchyme in various parts of the embryo, and these local vessels sprout, grow, and become united to form the continuous vascular system. The endothelium which forms the walls of all capillaries and the lining tissue of all blood vessels of larger dimensions forms directly from mesenchyme. Addition to this mesenchyme may occur by proliferation from endothelium already formed or by the conversion of mesenchyme as single cells or cellular aggregates (McClure, ’21; Reagan, ’17).

A second school which advocates the local origin of blood vessels differs from the view described above principally by the assumption that, while the endothelium of blood vessels appears to arise in loco from the mesenchyme, it is not a generalized type of mesenchyme but rather a “slightly modified mesenchymal cell” (Stockard, ’15). Relative to this position, the following quotation from Stockard, ’15, p. 323, is given:

The facts presented seem to indicate that vascular endothelium, erythrocytes and leucocytes, although all arise from mesenchyme, are really polyphyletic in origin: that is, each has a different mesenchymal anlage. To make the meaning absolutely clear, I consider the origin of the liver and pancreas cells a parallel case. Both arise from endoderm, but each is formed by a distinctly different endodermal anlage, and if one of these two anlagen is destroyed, the other is powerless to replace its product.

3. Later Development of Blood Vessels

While the capillary possessing a wall composed of thin, flattened endothelial cells is the basic or fundamental condition of all blood vessels in the body, it is only of transitory importance in the development of the arteries and veins. For, in the formation of the arteries and the veins, the primitive capillary enlarges and its endothelial wall is soon reinforced by the addition of white and elastic connective tissue fibers and smooth muscle tissue. The connective tissue and smooth muscle develop from the adjacent mesenchyme present in the area in which the capillary makes its appearance.

a. Arteries

The arteries are the system of blood vessels which convey the blood from the heart to the systemic organs. Most arteries are composed of three coats of tissue which come to surround the endothelium of the capillary, namely, an inner tunica intima, a middle tunica media, and an outer tunica adventitia. The tunica media is composed of smooth muscle fibers and elastic connective tissue fibers, while the other two coatings are fabricated of connective tissue fibers.

In the large arteries in the immediate vicinity of the heart, the tunica media is poorly muscularized but its elastic fibers are plentiful. However, in the more distally placed arteries, the so-called distributing arteries which include most of the arteries, the tunica media is supplied copiously with smooth muscle fibers.

6. Veins

The veins are the vascular tubes which convey the blood from the systemic organs back to the heart. The walls of the veins are more delicate than those of the arteries, and the various tunics mentioned above are thinner, especially the tunica media. The veins of the extremities form internal, pocket-shaped valves which prevent the blood from moving backward.

c. Capillaries

The capillaries which form the ramifying bed of blood vessels between the arteries and veins retain the primitive condition, and their walls are composed of flattened endothelial cells. The size of the arteries and the thickness of the arterial walls decrease as they approach the capillary bed, while those of the veins increase as they leave the capillary area.

4. Hematopoiesis (Hemopoiesis) a. Theories of Blood-cell Origin

Hematopoiesis is the name given to the process which effects the formation of blood cells. Though it is agreed that blood cells generally arise from mesenchymal cells, all students of the problem do not concur in the belief that all arise from a specific type of mesenchymal cell. For example, in the quotation given above from Stockard, T5, it is stated that one type of mesenchymal cell gives origin to the red blood cells, while leukocytes or white blood cells arise from a slightly different type of mesenchymal cell. This may be called the dualistic theory of hematopoiesis. The view held today by many in this field of development is that all blood cells arise from fixed, undifferentiated, mesenchymal cells which give origin to a mother cell, the hemocytoblast. From the hemocytoblast, four main stem cells arise, lymphoblasts, monoblasts, granuloblasts, and erythroblasts, each of which differentiates into the adult type of blood cell as shown in fig. 33 3 A. Such an interpretation is the basis for the monophyletic or Unitarian theory of blood cell origin. Some observers, however, believe that the erythrocyte, granulocyte, and the monocyte each have a separate stem cell. The latter view is the basis of the trialistic theory. (Consult Maximow and Bloom, ’42, pp. 107-116 for discussion relative to blood-cell origin.)

b. Places of Blood-cell Origin

1) Early Embryonic Origin of Blood Cells. It long has been recognized that the yolk-sac area is a region of early blood-cell development. This is one aspect of the angioblast theory of His, referred to on page 731. In the teleost fish, Fundidus, Stockard (’15) reports the origin of red blood cells from two main sources:

( 1 ) an intermediate celt mass or blood string in the vicinity of the notochord and

(2) the blood islands in the yolk sac.

However, the yolk-sac area appears to be the primary source for the early phases of hematopoiesis in most vertebrate embryos. In the human embryo, both red and white cells have been described as arising from primitive hemocytoblasts in the yolk sac by Bloom and Bartelmez ('40). These authors report the origin of primitive erythrocytes as arising primarily intra-vascularly, although some develop extra-vascularly. Definitive erythrocytes develop, according to these authors, in the entoderm and within blood vessels of the yolk sac (fig. 333B). In the 24-hr. chick embryo, the blood islands in the area vasculosa of the blastoderm show a direct conversion of mesodermal cells into primitive blood cells and the endothelium of the forming blood capillaries (fig. 333C). In the frog, blood islands appear in the mesoderm and entoderm of the ventro-lateral areas of the body of 3- to 4. 5 -mm. embryos. These islands are extensive, extending from the liver area caudally toward the tail-bud region.

2) Later Sites of Blood-cell Formation. As indicated previously in teleost fishes, early blood formation occurs in the region of the notochord near the developing kidney tissue, as well as in the yolk-sac area. During later development, hematopoiesis in teleost fishes is centered in the kidney area. The origin of blood cells from kidney tissue also is true in the amphibian tadpole (Jordan and Speidel, ’23, a and b). The liver also functions in these forms to produce blood cells. In the developing shark embryo, blood cells appear to be formed around the heart and later in the esophageal area of the adult. In the adult frog, the spleen functions as a center of blood-cell formation, although in the

Fig. 333. Developing blood cells. (A) Diagram showing origin of different types of blood cells from the primitive hemocytoblast. (Redrawn and slightly modified from Patten, 1946. Human Embryology, Blakiston, Philadelphia.) (B) Blood-cell origin in the yolk-sac area of human embryo. (Redrawn from Bloom and Bartelmetz, 1940. Am. J. Anat. 67.) (C) Differentiation of blood cells and blood vessel endothelium in a

blood island of chick embryo yolk-sac area.

terrestrial form, Rana temporaria, the bone marrow functions in this capacity as it does in the adults of reptiles, birds, and mammals. In the adult reptile and bird, the bone marrow seems to function in the production of all types of blood cells. In the mammal, the bone marrow possibly elaborates only erythrocytes and granular, white blood cells, while the lymphocytes probably are produced in other areas, such as the pharyngeal and palatine tonsils and lymph nodes, etc. In all vertebrates from the teleost fishes to the mammals, it is probable that scattered lymphoid tissue in various parts of the body functions in the formation of lymphocytes.

During the development of the early human embryo and later fetus, the following have been given as sites of blood -cell formation (Minot, ’12; Gilmour, ’41):

(a) yolk sac in embryos up to 3 mm., i.e., the end of the fourth week of pregnancy,

(b) mitosis of previously formed erythroblasts in general circulation, yolk sac, and chorion of embryos from 3 to 9 mm. in length,

(c) liver and yolk sac of 10- to 18-mm. embryos. In embryos of 470- to 546-mm. there is a gradual decrease in the liver,

(d) spleen, beginning in the 28-mm. embryo; thymus, and lymph glands in the 35-mm. and larger embryos,

(e) bone marrow during the third month and later.

3) Characteristics of Development of the Erythrocyte. Most vertebrates in the adult condition retain the nucleus in the erythrocyte or red blood cell. To this cell is given the function of carrying oxygen from the site of external respiration to the body tissues. It also is a factor in conveying carbon dioxide from the tissues to the site of external respiration. The oxygen-carrying capacity of the erythrocyte resides in the presence of the compound hemoglobin. Hemoglobin is a complex protein molecule, containing iron atoms. The iron atoms make it possible for the hemoglobin to convey oxygen.

In the adults of various amphibian species, there is a tendency for the red blood cell to lose its nucleus by various means (Noble, ’31, pp. 181-182). This tendency toward loss of the nucleus reaches an extreme form in Batrachoseps where more than 90 per cent of the red blood cells have lost their nuclei. In adult mammals, the mature erythrocyte loses its nucleus (column 6, fig. 333A) but it is retained in the early embryo.

4) Characteristics of Various White Blood Cells. White blood corpuscles or leukocytes vary greatly in number and in morphological features in all vertebrates. In general, the following two major groups of white blood corpuscles may be distinguished.

a) Granulocytes. Granulocytes are cells which arise from granuloblasts (columns 3, 4, and 5, fig. 333A). These cells are characterized by the presence of an irregularly shaped nucleus and by a cytoplasm which possesses granules of various dimensions and staining affinities.

b) Lymphoid Forms. Lymphoid forms are of two types, namely, lymphocytes and monocytes. These cells arise from lymphoblasts and monoblasts respectively (columns 1 and 2, fig. 333A). The lymphocytes are small, rounded cells with a clear cytoplasm and a large nucleus. They are found in all vertebrates and are abundant especially in fishes and amphibia. Large numbers are found in the lymph nodes in various parts of the body. Monocytes are similar to the lymphocytes but are much larger and have a tendency to possess an irregularly shaped nucleus. Various hematologists hold that the monocyte is a special type of blood cell, distinct from other leukocytes and of a separate developmental origin.

D. Morphogenesis of the Circulatory System

1. Introduction

The major alterations of the basic arterial and venous conditions into the morphology present in the adult or definitive body form of the species occur during the larval period, or the period of transition from primitive embryonic body form to the definitive or adult form. This fact is true not only of the circulatory system but of all other organ systems as well (Chap. 11). The pronounced changes, therefore, which occur in the revamping of the basic, generalized condition of the circulatory system during the larval period should be regarded as transformation which adapts the basic embryonic condition to conditions which must be met when the developing organism emerges into the environment of the adult.

2. Transformation of the Converging Veins of the Early Embryonic Heart into the Major Veins which Enter the Adult Form of the Heart

a. Alteration of the Primitive Converging Veins of the Heart in the Shark, Squalus acanthias

An early stage of the developing venous circulation of Squalus acanthias is shown in figure 3 34 A. Only two veins are present, the primitive vitelline veins. They enter the sinal rudiment of the developing heart. Before the liver lobes form, the left vitelline vein develops a new venous sprout, the intestinal vein, which extends caudalward along the lateral aspect of the intestine to the developing cloacal area (fig. 334B). Here it forms a collar-like venous structure around the cloaca and continues back below the tail gut as the caudal vein. Meanwhile, the anterior, posterior, and common cardinal veins begin their development, and the liver also begins to form (fig. 334C). As the liver develops, two prominent liver lobes are elaborated (Scammon, T3 and the vitelline veins become surrounded by the developing liver trabeculae (Chap. 13). During this process, the vitelline veins are fenestrated, and sinusoids are produced. These sinusoids connect with the right and left vitelline (hepatic) veins at the anterior end of the liver.

Posterior to the liver, the right and left vitelline veins form a collar around the duodenum as shown in figure 334C. The left portion of the duodenal collar then disappears, and the hepatic portal vein which receives blood from the developing stomach, pancreas, and intestine enters the liver as indicated in figure 334D.

As the above development progresses, three important changes are effected (fig. 334E):

( 1 ) The lateral veins along the lateral body wall arise and join the common cardinal veins near the entrance of the right and left vitelline (hepatic) veins;

(2) the intestinal vein loses its connection with the caudal vein; and

(3) the postcardinal veins extend caudally and connect with the caudal vein.

Meanwhile, the mesonephric kidneys begin to develop, and new veins, in the form of irregular venous spaces, form between the two kidneys. These new veins are the subcardinal veins. The subcardinal veins are joined by the internal renal veins which ramify through the kidney substance from the posterior cardinal veins. They course over and around the forming renal tubules (fig. 334F, G).

Later, the two subcardinal veins extend forward and by means of an anastomosis on either side connect with the posterior cardinal veins anterior to the mesonephric kidneys. As this transformation occurs, the segment of each posterior cardinal vein atrophies between the kidney and the point where the subcardinal venous anastomosis joins the posterior cardinal vein (fig. 334G).

While the above changes evolve, the anterior cardinal veins expand greatly over the dorsal pharyngeal area, where they form sinus-like spaces. These anterior cardinal venous sinuses receive the internal jugular veins from the brain region and various pharyngeal veins. Coronary veins and external Jugular veins also develop as shown in figure 334H.

b. Changes in the Primitive Converging Veins of the Heart in the Anuran Amphibia

1) Vitelline Veins. As in the shark embryo and in all other vertebrates, the vitelline veins of the frog or toad embryo are among the first blood vessels to be formed in the body. In frog embryos of about 3- to 4-mm. in length, the two vitelline veins begin to appear as irregular blood spaces along the ventro-lateral aspect of the midgut region, extending anteriad around the forming liver. At a point immediately anterior to the liver rudiment, these vessels fuse to form the endocardinal rudiment of the heart (fig. 332I-K).

Proceeding forward from the heart region, the two primitive subintestinal blood vessels continue forward below the rudiment of the foregut where they form the rudiments of the ventral aorta. They diverge and extend dorsad around the foregut to the dorsal area of the foregut. These vessels which thus pass around the foregut represent the third pair of aortal arches, i.e., the first pair of branchial aortal arches (fig. 335A). The first branchial aortal arches join the forming dorsal aortae. The dorsal aortae form first as irregular blood spaces, extending along the primitive gut from below the forming brain posteriad to the midgut area. Here they diverge to give origin to the vitelline arteries which ramify over the yolk substance of the midgut and there anastomose with branches of the vitelline veins.

About the time of hatching, the two vitelline veins become enmeshed in the substance of the developing liver, and the vitelline veins gradually become divided into three groups (fig. 335B):

(a) a right and left vitelline vein between the liver and the sinus venosus of the heart,

(b) the veins within the liver which form an irregular mesh work, and

(c) the two vitelline veins, posterior to the liver substance.

The left vitelline vein, anterior to the liver, soon atrophies and becomes fused with the right vitelline vein as indicated in figure 335C and D. The right vitelline vein thus receives the hepatic veins. Within the liver substance, the two vitelline veins break up into smaller veins to form ultimately the sinusoids of the liver (fig. 335C). Posterior to the liver, the vitelline veins form the hepatic portal and intestinal veins (fig. 335C).

2) Lateral (Ventral Abdominal) Veins. The lateral veins form first as two minute veins, which extend posteriad from the lateral ends of the sinus venosus of the heart. Eventually they unite with the iliac veins as shown in figure 335D.

Fig. 334. The developing venous system in Squalus acanthias. (Modified from Hochstetter, ’06.) (A) An early stage in the development of the venous system. The two

primitive vitelline veins only are present. (B) Later stage in development of vitelline veins. (C) Early stage in development of hepatic portal system. A venous ring is formed around the duodenum. Anterior and posterior cardinal veins are evident. (D) Later stage in the hepatic-portal system development. Left segment of duodenal collar has disappeared. Observe that the efferent hepatic veins (V. hepaticae revehentes) represent the right and left vitelline veins between the liver lobes and the sinus venosus, whereas the afferent hepatic veins (V. hepaticae advehentes) are the vitelline veins just posterior to the liver. (E) Lateral veins make their appearance. Posterior cardinal veins join veins around the cloacal area and thus assume responsibility for venous drainage of the tail region, and the intestinal vein in consequence loses its connection with the caudal vein of the tail. (F) Subcardinal veins appear between the kidneys. (G) Subcardinal veins make connection with posterior cardinal veins. Posterior cardinal veins regress anterior to the mesonephric kidneys where the posterior cardinal and subcardinal veins anastomose. (H) Mature plan of the venous system showing the converging veins of the heart. Hepatic portal vein omitted.

Anteriorly, the two lateral (ventral abdominal) veins lose their connection with the sinus venosus and merge together to form one ventral abdominal vein; the latter acquires a connection with the hepatic portal vein near the liver. A ventral abdominal circulation is established thus between the hepatic portal system and the iliac veins (fig. 335E, F).

3) Formation of the Inferior Vena Cava. The inferior vena cava is a vessel not found in the venous system of the developing shark. It is a blood vessel associated with and characteristic of lung breathers. As such, the inferior vena cava appears first among the vertebrates in the lungfishes (Dipnoi) and it functions to shunt the blood from the posterior regions of the body over to the right atrial portion of the heart. That is, the inferior vena cava is a vessel correlated with the division of the heart into two parts. One part is devoted to getting the non-oxygenated systemic blood into the lung region, while the other part functions to propel the aerated blood from the lungs into the head region and other parts of the body. This division of labor within the heart is not necessary in strictly gill-breathing fishes, such as the sharks and teleosts, and, in consequence, an inferior vena cava is not developed in these vertebrates.

The formation of the inferior vena cava in the anuran amphibia is shown in figure 335C-G and need not be explained further. It is to be observed that it forms from four segments:

( 1 ) a right vitelline vein,

(2) an hepatic segment,

(3) a segment which extends posteriad from the liver to the fused subcardinal vein, and

(4) the subcardinal vein, (Consult figure 335E.)

4) Formation of the Renal Portal System. The renal portal system is inaugurated among the cartilaginous fishes (i.e., the shark group). It does not exist in cyclostomes. As shown in figure 334 relative to the developing shark embryo, it results from the formation of the subcardinal veins, accompanied by the obliteration of the anterior portions of the posterior cardinal veins.

Fig. 335. Developing venous vessels in the anuran amphibia. (B-G, redrawn and modified from Kampmeier, 1920, Anal. Rec. 19; H, redrawn from Kampmeier, 1925, J. Morph. 41; I, redrawn from Goodrich after Kerr, 1930, Studies on the Structure and Development of Vertebrates, Macmillan, Ltd., London.) (A) Primitive plan of early circulation in frog embryo. The relationship of the primitive venous system shown in B to the rest of the vascular system is evident. (B) Plan of venous system of 4 mm. embryo of the toad, Bufo vulgaris. (C) Plan of venous system of 6 mm. embryo of the toad, Bufo vulgaris. (D) Plan of venous system of 15 mm. embryo of the toad, Bufo lentiginosus. (E) Plan of venous system of 18 mm. embryo of the toad, Bufo lentigirtosus. (F) Plan of venous system of young toad of Bufo lentiginosus, immediately after metamorphosis. (G) Plan of venous system of mature Rana pipiens. (H) Left posterior lymph hearts of an adult Rana pipiens. (1) Internal structure of mature frog heart.

The blood from the tail and posterior trunk region of the body thus must pass through the small blood vessels within the kidney substance. Here waste materials and excess water are extracted before the blood is passed on to the heart and aeration systems. The renal portal system is developed exceptionally well in the embryos and adults of fishes and amphibia. It is inadequately developed in the adult reptile, and it is questionable whether or not the poorly developed, renal portal system functions in the adult bird. The adult mammal does not possess this system. However, the embryos of all reptiles, birds, and mammals possess a renal portal system wherein blood is shunted through the kidney substance from the posterior cardinal veins into the subcardinal complex. It is a most transient affair in the mammalian embryo. The development of the renal portal system in the anuran embryo is shown in figure 335C-E. Observe that pronephric and mesonephric renal portal systems are developed.

5) Precaval Veins. The formation of the precaval veins is shown in figure 335B-G. It is to be observed that the common cardinal veins become transformed into the anterior or precaval veins, while the anterior cardinals persist as the internal jugular veins.

c. Changes in the Primitive Converging Veins of the Heart in the Chick

1) Transformation of the Vitelline and Allantoic Veins: a) Vitelline Veins. The vitelline veins in the developing chick first make their appearance as two delicate capillaries, one on either side of the inner wall of the anterior intestinal portal in blastoderms of 26-28 hours of incubation. At this time there are about four pairs of somites present. These minute blood vessels are intimately associated with the entoderm of the anterior intestinal portal, and eventually come to lie side by side immediately below the foregut as the anterior intestinal portal recedes caudally. At about 27-29 hrs. of incubation, or when the embryo has about five to six pairs of somites, the two splanchnic layers of the hypomeric mesoderm, in the area where the heart is to form, begins to cup around and enclose the two vitelline capillaries (fig. 332L). A little later, at about 29-33 hrs. of incubation, these two splanchnic mesodermal layers begin to fuse above and below the vitelline capillaries (fig. 332M). At 33-38 hrs. of incubation, or when nine to ten pairs of somites are present, a simple, tubular heart is present which contains the rudiment of the endocardium within in the form of the two fused or fusing vitelline capillaries. This endocardial rudiment is enclosed by the hollow, tube-like epimyocardial rudiment derived from the fused layers of splanchnic mesoderm (fig. 336A).

At about 33-38 hrs. of incubation (fig. 336A), the primitive circulatory system consists of the following:

(1) Two vitelline veins which converge to enter the forming heart just anterior to the intestinal portal;

(2) the primitive tubular heart;

(3) two delicate capillaries, the future ventral aortae, course anteriad from the heart below the foregut. As the ventral aortae approach the anterior limits of the foregut they diverge and travel dorsad as the mandibular aortal arches, one on either side of the gut tube, to the dorsal region. In the dorsal area of the foregut the mandibular aortal arches become continuous with

(4) the dorsal aortae. These two delicate vessels lie upon the foregut on either side of the notochord, and extend caudalward into the region of the developing midgut.

During the period of 40 to 50 hours of incubation the following changes occur in the above system (fig. 336B and B'):

( 1 ) The rudimentary vitelline arteries extend outward over the yolk-sac area from the dorsal aortae, forming many small capillaries.

(2) The anterior and posterior cardinal veins and connecting intersegmental veins are established and unite with the sinus venosus by means of the common cardinal vein (fig. 336B').

(3) The vitelline veins extend outward over the blastoderm and continue anteriorly around the head area as the anterior vitelline veins. The latter veins unite with the circumferential blood sinus. A complete circulation through the embryo and out over the yolk-sac area is thus effected.

During the early part of the third day of incubation the right and left vitelline veins begin to fuse in the area just posterior to the heart. This fusion forms a single vein, the ductus venosus (fig. 337A). The latter structure joins the sinus venosus of the heart. Posteriorly, the vitelline veins make a secondary connection with the developing posterior vitelline or omphalomesenteric veins which extend backward along the sides of the midgut to the area where the vitelline arteries leave the dorsal aortae. At this point each omphalomesenteric vein turns sharply laterad and courses along the pathway of a vitelline artery (fig. 336C).

At the end of the third day of incubation the ductus venosus is present as an elongated structure lying between the anterior intestinal portal and the heart. A posterior vitelline vein continues posteriad from the ductus venosus around each side of the anterior intestinal portal (fig. 336D). As observed in Chapter 13, during the third and fourth days of incubation the liver rudiment begins to form. In doing so, the trabeculae of the liver surround the ductus venosus. The immediate segment of the ductus venosus which becomes surrounded by the forming liver substance forms the meatus venosus. As development of the liver proceeds, two main groups of veins develop in the liver substance (fig. 337B, D): (1) An anterior efferent group of hepatic veins which drain blood from the liver and (2) a posterior afferent set of hepatic

Fig. 336. Early development of the circulatory system in the chick. (A) Primitive vitelline (omphalomesenteric) veins, heart, ventral aorta, and the first or mandibular pair of aortal arches. About stage 10 of Hamburger and Hamilton, 1951, J. Morph. 88. Approximately 33-38 hrs. of incubation. (A') Lateral view of same. (B) Lateral view of chick circulatory system of about 45-50 hrs. of incubation. (About Hamburger and Hamilton stage 13.) (B') Same, showing common cardinal vein (duct of Cuvier).

(C) Circulatory system of chick during early part of third day of incubation. (About Hamburger and Hamilton stage 15.) (D) Circulatory system of chick embryo about

72 hrs. incubation.

veins, representing branches of the hepatic portal vein. The latter brings blood from the stomach and intestinal areas to the liver.

During the fifth to seventh days of incubation, the afferent and efferent sets of hepatic veins develop profuse branchings, and venous sinusoids are formed within the liver substance between these two sets of veins. Meanwhile, the meatus venosus within the liver atrophies and a complete hepatic portal system is established between afferent and efferent hepatic veins during the seventh and eighth days of incubation as shown in figure 337E.

While the above changes in the liver are emerging, changes in the omphalomesenteric veins, posterior to the liver substance, are produced as shown in figure 337A-E. By the fifth day, a new vein, the mesenteric vein, is formed (fig. 337D), which begins to drain blood from the developing midgut and hindgut areas. By the eighth day, the mesenteric vein is a prominent structure (fig. 337E). At this time, the blood from the yolk sac, via the omphalomesenteric veins, and that from the mesenteric vein must pass through the liver sinusoids en route to the efferent hepatic veins (fig. 337E).

b) Allantoic Veins. The two allantoic or lateral veins begin to develop during the third day of incubation, and, by the end of this day, two delicate blood vessels extend along the lateral body wall, reaching back toward the hindgut area (figs. 336D; 337B). During the fourth day (fig. 337C), the caudal ends of the two allantoic veins begin to ramify within the walls of the allantois. A secondary attachment to the hepatic veins within the liver is established also at this time (fig. 337C). During the late fourth day and the fifth day of incubation, the right allantoic vein degenerates, and the proximal portion of the left allantoic vein loses its connection with the common cardinal vein (fig. 337D). During the seventh and eighth days (and until the time of hatching), the passage of blood from the allantois through the liver to the vena cava inferior is as indicated in figure 337E. The portion of the allantoic vein extending anteriorly from the umbilical area to the liver persists after hatching and drains blood from the midventral portion of the body wall. It is called the epigastric vein (fig. 3371).

2) Formation of the Inferior Vena Cava. The formation of the inferior vena cava of the chick is shown in figure 337F-I and needs no other explanation. It is to be observed that, following the degeneration of the mesonephric kidneys and the ascendancy of the metanephric kidney, the passage of blood by way of the renal portal system through the mesonephric kidney is abated. In the newly hatched chick, a much-weakened, renal portal system is established via the renal portal vein (fig. 3371J However, most of the blood through this vein passes directly into the common iliac vein and not through the kidney substance.

3) Development of the Precaval Veins. The precaval veins are the direct descendants of the anterior cardinal and common cardinal veins as indicated in figure 337F-I. In figure 3371, it is to be observed that the caudal ends of

Fig. 337. Ventral views of developing allantoic, hepatic portal, and inferior caval veins in chick. (Diagrams C and D are adapted from figures in Lillie, 1930, The Development of the Chick, Henry Holt, N. Y., after Hochstetter; diagrams F-H are adapted, considerably modified, from Miller, 1903, Am. J. Anat. 2.) (A) Diagram of converging veins

of heart during early third day of incubation. (B) Same at end of third and early fourth days. (C) Middle fourth day. (D) End of fourth and early fifth days. (E) Seventh to eighth days. (F) Development of inferior vena cava at end of fourth and beginning of fifth day of incubation. (G) Same, 6-7 days. (H) Same, fourteenth day. (I) Same at about hatching time, 20-21 days.

the posterior cardinal system function to drain the blood from the caudal end of the body and posterior appendages, while the anterior cardinal veins and common cardinal veins function to drain the blood from the head, neck, and forelimb areas.

d. The Developing Converging Veins of the Mammalian Heart (e.g., Human)

The formation of the hepatic portal system in the human embryo is shown in figure 338G, H, and that of the inferior and superior venae cavae is shown in figure 338 A-F. The general principles of venous development, described in the previous pages of this chapter, apply here, and descriptive matter is not needed to supplement the accompanying figures. It is worthy of mention, however, that two additional veins are introduced in the abdominal area of the embryo, namely, the two supracardinal veins. These veins persist as a part of the vena cava inferior and azygos veins. Anteriorly, the two precavae, so prominent in the lower vertebrates, including the birds, are displaced partially by the formation of an anastomosing vein from the left to the right side with the dropping out, to a considerable extent, of the proximal portion of the left precava. Thus, the common cardinal vein on the right side comes to function as the proximal portion of the single superior or anterior vena cava, while the common cardinal vein on the left side comes to form the coronary sinus of the heart, and occasionally as a variant, the oblique vein of the left atrium.

3. Development of the Heart a. General Morphology of the Primitive Heart

In the vertebrate group, two types of hearts are present, namely, lymp h hearty {fig. 335H) and the heart of the arteriovenous system. The heart of the arteriovenous system is a centralized, well-muscularized mechanism, placed ventral to the esophageal segment of the gut in the anterior extremity of the coelomic cavity. Its function is to receive blood from the veins of the body and to propel it forward toward the anterior or head region. Fund amen tally, the ern bryon ic Jieart of the arteriovenous system is a tubular affair, composed of four segments:

(1) a thin-walled sinus venosus or caudal portion of the heart, connecting with a series of converging veins,

(2) the atrium, a segment lying anterior to the sinus,

(3) the ventricle, lying anterior to the atrium, and

(4) the bulbus cordis.

The ventricle and, to some extent, the bulbus cordis of the embryonic heart later develop the structures which act as the main propulsive mechanism of the heart, while Ihe sinus and atrium give origin to the blood-receiving areas.

b. The Basic Histological Structure of the Primitive Embryonic Heart

Structurally, the embryonic heart is composed of two parts. An inner delicate lining, the rudiment of the endocardium, forms as a result of the fusion of the vitelline blood capillaries in the immediate area of the forming heart. The endocardium thus is composed of endothelium (fig. 332F-M). Surrounding the endocardial rudiment, there is the epimyocardium derived from the ventro-mesial portions of the hypomeric (splanchnopleural) mesoderm which extends ventrally from the foregut in this area (fig. 332F-M). Basically, the mesial walls of the two hypomeric areas of the mesoderm which lie below the foregut in this region constitute the ventral mesentery of the primitive gut. Consequently, the epimyocardium of the primitive heart may be regarded as modified ventral mesentery. That portion of the ventral mesentery which is dorsal to the forming heart forms the dorsal mesocardium, while that part which extends ventrally below the heart forms the ventral mesocardium. The latter is a transient structure, no sooner formed than obliterated in most instances. The dorsal mesocardium tends to persist for a time, more in some species than in others. Caudally, the posterior lateral areas of the sinus venosus project the splanchnopleural mesoderm laterally to contact the lateral somatopleural mesoderm with which the splanchnopleural mesoderm fuses. This outward extension of the caudo-lateral edges of the sinus venosus produces a bridge across the coclomic space from the lateral body wall to the sinus venosus. These bridges on either side across the primitive coelom form the lateral mesocardia. Through these mesocardial bridges, the common cardinal veins empty their contents into the heart.

Fig. 338. Changes in the converging veins of the heart in the mammalian embryo. (Redrawn and modified from Patten, 1946, Human Embryology, Blakiston, Philadelphia, after McClure and Butler.) (A F) Developmental changes in converging veins of the human heart. Primitive converging veins of the heart shown in black; hepatic segment of inferior vena cava shown in white with coarse stipple; subcardinal veins shown in light stipple; supracardinal veins in white with crossed lines. (Note: the author assumes the responsibility for adding a vitelline venous segment to the anterior end of the developing inferior vena cava. As a result of observations on developing pig, cat, and opossum embryos, the author is convinced that a vitelline segment is contributed to the developing posterior vena cava in the mammal.) (A) Primitive basic condition. (B-F) Later stages as indicated. (F) Adult condition. The following contributions appear to enter into the formation of the inferior vena cava, viz., (1) a very short vitelline segment; (2) an hepatic segment; (3) an anastomosis between the hepatic segment and the subcardinal interrenal anastomosis; (4) a subcardinal-supracardinal anastomosis; (5) a right supracardinal segment caudal to the kidneys; and (6) a posterior cardinal contribution in the pelvic area. Note also that the azygos vein is formed from the anterior end of the right posterior cardinal vein plus the right supracardinal with its connections with the hemiazygos vein. Observe further that the superior vena cava is composed of the right common cardinal vein from the area of juncture with the azygos vein to the point of its entrance into the right atrium. (G-J) Formation of the hepatic portal vein in the pig. (Redrawn and slightly modified from Patten, 1948. Embryology of the Pig, Blakiston, Philadelphia.

c. Importance of the Septum Transversum to the Early Heart

There is another structure which is important to the primitive embryonic heart and to its later development. This structure is the primary septum transversum or the mesodermal partition which forms across the coelomic cavity, below (ventral) to the lateral mesocardia. It forms not only a partition or bulwark, separating the developing liver substance from the primitive heart, but it is also a suspensory ligament for the caudal end of the sinus venosus and the converging veins of the heart. (See Chap. 20.)

d. Activities of Early-Heart Development Common to All Vertebrates

The early stages of heart development, following the formation of the basic rudiments mentioned above, are essentially the same for all vertebrates. These changes, which result in the formation of a sigmoid or S-shaped structure, are as follows (see figs. 336, 339):

( 1 ) The dorsal mesocardium soon disappears for most of its extent, and the primitive heart tube begins to elongate and to change its shape rapidly.

(2) The ventricular portion bends ventrally and to the right and, at the same time, grows posteriad, becoming thick-walled.

(3) The atrial area expands laterally, grows forward dorso-anteriad over the ventricular area; and at the same time forms two lateral lobes.

(4) The sinus venosus remains thin walled and rigidly attached to the septum transversum. The latter, in all vertebrates above the fishes, bends forward along its upper margins during the early period of development.

(5) The bulbus cordis extends slowly and becomes a thickened anterior continuation of the heart from which arise the ventral aortic roots.

e. Development of the Heart in Various Vertebrates

From the generalized, S-shaped, basic condition, the hearts of the various vertebrate groups begin to diverge in their development as follows:

1) Shark, Squalus acanthias. Starting as a straight tube when the embryo is 5.2 mm. long (fig. 339A), the ventricular portion begins to bend toward

Fig. 339. Early stages in morphogenesis of various vertebrate hearts. (A-C) Stages in heart development in Squalus acanthias. (Redrawn from Scammon, 1911, Chap. 12, in Normentafeln Entwichlungsgeschichte der Wirbeltiere by F. Keibel, G. Fischer, Jena.) (I>-F') Heart development in the frog, Rana pipiens. (D-F) Left lateral views; (F') ventral view. (G-K) Heart development in the chick, ventral views. (H-K, redrawn from Kerr, 1919, Text-Book of Embryology, vol. 11, Macmillan and Co., Ltd., London, after Greil.) (L- O) Heart development in the human embryo, ventral views. (Redrawn from Kramer, 1942, Am. J. Anat. 71. L, after Davis, modified; M, after Tandler, modified; N, after Waterston, modified.) Observe that ventricular end of the original bulbus cordis, i.e. the conus portion, contributes to the right ventricle in diagrams N and O.









artery V right


^ ROOT / T



Fig. 339. (See facing page for legend.)




the right and ventrad in the embryo of 7.5 mm. At 15 mm., the heart appears as indicated in figure 339B, while, at 20.6 mm., it assumes the general appearance of the adult form (fig. 339C). It is to be noted that the ventricular portion of the heart does not bend as dramatically toward the right as in the chick or mammalian heart. In the embryo of 37 mm., the heart already has attained the characteristics of the adult form. The following developmental features are present. The bulbus cordis has transformed into the anterior contractile chamber, the conus arteriosus; the ventricular area has developed a pronounced musculature; the atrium is thin walled and bilobed, while the sinus venosus is cone shaped with its base applied against the septum transversum. Right and left valves guard the sinu-atrial entrance. A series of semilunar or pocket valves arc arranged around the atrioventricular orifice, while, more anteriorly, cup-shaped valves are forming in transverse rows along the inner walls of the conus arteriosus.

2) Frog, Rana pipiens. At 4'/i mm. in length, the heart is present as a simple straight tube (fig. 339D). At 5 mm., it begins to bend, the ventricular area moving ventrad and toward the right, and the atrial area and sinus venosus moving anteriad over the ventricular area (fig. 339E). At 7 mm., the heart has assumed the typical S-shaped condition of the adult form, and constrictions appear between the atrium and ventricle (fig. 339F). At this time, also, a median septum begins to divide the atrial chamber. The atrial septum begins as a fold from the antero-dorsal wall of the atrium and grows ventrad and posteriad to divide the atrium into a larger right atrium and a smaller left artium. Moreover, as the atrial septum is developed, it forms to the left of the opening of the sinus venosus into the atrium. Therefore, in the 8- to 10-mm. tadpole, the opening of sinus venosus into the atrium is entirely restricted to the right atrium, and the flow of venous, systemic blood is directed toward the right side of the heart. At about this time, also, the formation of the vena cava inferior proceeds rapidly. (See fig. 335.) At 8 to 10 mm., the lung buds (Chap. 14) expand rapidly, and the pulmonary veins begin to bring back blood from the lungs. The pulmonary veins empty into the left atrium (fig. 257B).

During the late tadpole stages and metamorphosis, internal changes occur which transform the heart into a complicated mechanism, designed to separate and project the oxygenated blood anteriad toward the head and into the systemic vessels; the non-oxygenated blood from the sinus venosus passes into the pulmocutaneous arteries. These different blood currents within the heart are made possible largely by the modification of the internal walls of the primitive bulbus cordis into the highly complicated mechanism of the contractile conus arteriosus. Aside from a series of small pocket valves, the dorsal wall of the conus forms an elongated spiral valve which functions to separate its channel into two parts. The non-oxygenated blood is projected dorsally to the spiral valve and into the pulmocutaneous vessels by the spiral



valve, while the oxygenated blood passes ventrally to the spiral valve and into the arteries coursing toward the head and into the systems (fig. 3351). This condition of the conus is present also in urodeles with well-developed lungs, but, in urodeles without well-developed lungs, the spiral valve is absent and the interatrial septum may regress (Noble, ’31, pp. 187-194).

3) Amniota. The heart of reptiles, birds, and mammals differs from the heart of the Amphibia in that a mechanism is present which separates, more or less completely, the oxygenated blood from the non-oxygenated blood. For example, the heart of birds and mammals is a four-chambered affair as an interventricular septum divides the primitive ventricle into two separate compartments while an interatrial septum separates the primitive atrium into two atria. A double heart is produced in this manner wherein the nonoxygenated blood returning from the organ systems passes through the right atrium and ventricle en route to the lungs while the oxygenated blood from the lungs journeys through the left atrium and ventricle on its way back to the organ systems. In the heart of birds and mammals, it is to be observed also, that only two arterial channels convey blood from the heart; namely, a pulmonary arterial trunk and a systemic arterial trunk. Another feature is present in the heart of the birds and mammals which serves to distinguish it from the hearts found in all lower vertebrates, in that the sinus venosus is absorbed almost entirely during embryonic development into the wall and structure of the right atrium.

Turning now to a consideration of the hearts of reptiles we find that the turtles and snakes possess a heart with two atria and a ventricular region divided rather completely into two ventricles. However, the interventricular septum is slightly incomplete in the region near the atria, and some leakage of blood between the two ventricles is possible. In the crocodilians the interventricular septum is completely developed, but a small opening, the fommen of Panizza, is present at the bases of the two systemic arterial trunks. This foramen arises as a secondary perforation later in development and does not represent an incompleteness of the interventricular septum. In the reptilian heart the sinus venosus retains its identity as a separate chamber of the heart. Furthermore, contrary to the conditions found in the avian and mammalian heart, three arterial trunks convey blood away from the ventricles. Two of these vascular trunks come from the right ventricle, and one from the left ventricle, for a pulmonary trunk conveys blood from the right ventricle to the lungs, while a systemic aortic root also carries blood from the right ventricle to the abdominal aorta. From the left ventricle, on the other hand, blood is propelled through a single aortic root to the head, forelimbs, and abdominal aorta (fig. 341H).

a) Heart of the Chick. The heart arises as a simple tube during the second day of incubation (fig. 339G). At the end of the second day and during the third day, the primitive ventricle bends to the right, and the atrium



begins to travel forward above the ventricle (figs. 336C; 339^1"). At the end of the third day, the heart attains the typical sigmoid or S-shaped condition which arises as the first major step in heart development in all vertebrate embryos. During the fourth day of incubation, the atrial area expands into two main lobes, the beginnings of the right and left atria; the ventricular area expands greatly and thickens; and the bulbus cordis lies in the median line between the developing atria (fig. 3391). The position of the various parts of the heart on the whole assumes more nearly the adult condition.

Internally, toward the end of the fourth day, an interatrial septum begins to develop from the dorso-anterior area between the two atrial lobes, slightly to the left of the opening of the sinus venosus. The septum continues to form posteriad toward the narrowed atrio-ventricular opening between the atria and the forming ventricles. Simultaneously in the atrioventricular opening, two endocardial thickenings, the endocardial cushions, arise, one dorsal and one ventral. At the apex of the ventricle, an interventricular septum appears and grows forward toward the atrioventricular opening (fig. 340G).

During the fifth and sixth days, the two endocardial cushions grow together and separate the atrioventricular canal into two passageways by the formation of a cushion septum. The atrial septum grows toward the endocardial cushion area and unites with the cushion septum. However, the atrial septum never is completed during embryonic life, as small openings or fenestrae, appear in the septum permitting blood to pass through the septum. During the last week of incubation, the fenestral openings in the atrial septum become much smaller and completely close shortly after hatching. The ventricular septum, meanwhile, grows forward to unite with the cushion septum. Up to the fifth day, but one passageway leaves the heart via the developing bulbus cordis and ventral aorta. However, during the fifth day, beginning at the area just anterior

Fig. 340. Early stages in morphogenesis of various vertebrate hearts {Continued). (A-E) Internal changes in the developing heart of the pig. (A-D, redrawn from Patten, 1948. Embryology of the Pig, 3d edit., Blakiston, Philadelphia.) (A) Diagram of 3.7 mm. pig embryo heart, ventral wall removed. (B) Similar diagram of 6 mm. pig heart. (C) Similar diagram of 9.4 mm. pig heart. (D) Similar diagram of dissected pig fetal heart shortly before birth. (E) Schematic drawing of dissected 18 mm. pig heart viewed from right side with walls of right atrium and right ventricle removed. Observe that the bulbus cordis has divided into two vascular trunks. (F) Dorsal aspect of the heart of an 11 wk. (60 mm.) human embryo. (Redrawn and modified from Patten, 1946. Human Embryology, Blakiston, Philadelphia.) The contraction wave of the heart beat is indicated by heavy arrows. Starting at the sinus node situated in the dorsal wall of the right atrium, the contraction wave spreads over the atrial walls and also to the atrioventricular node located in the atrial septum from whence it travels distally through the ventricular tissue. (G) The developing chick heart, of about 6-7 days. Right walls removed to show developing cardiac septa. The ventricular septum is still incomplete, and the atrial septum is fenestrated. (This figure has been modified considerably from Kerr, 1919. Text-Book of Vertebrate Embryology, vol. 11, Macmillan, Ltd., London, after Greil.) (H) Adult heart of the South American lung fish, Lepidosiren paradoxus, right side removed. (Redrawn from Robertson, 1913. Quart. J. Micros. Sci., 59.)




Fig. 340. (See facing page for legend.)




to the sixth pair of aortal arches, a spiral septum begins to form within the caudal portion of the ventral aortal sac and the bulbus cordis. This septum grows caudalward within the bulbus in a spiral manner, separating the pulmonary trunk ventrally and the root of the systemic aorta dorsally. It continues backward toward the interventricular septum and there unites with a similar septum at the caudal end of the bulbus. The original bulbus cordis thus becomes divided at about the seventh day of incubation into two separate vessels which course spirally around each other, namely, a pulmonary trunk which unites with the right ventricle and an aortal root which is continuous with the left ventricle (fig. 339J).

Coincident with the above changes, the valves of the heart are developed. As the spiral septum is developed in the region of the bulbus cordis, three semilunar or cup-shaped valves appear at the base of each of the divisions of the bulbus. That is, at the base of the aortic root and also at the base of the pulmonary trunk. These valves prevent the backward flow of the blood from the aortic root into the left ventricle and from the pulmonary trunk to the right ventricle. When the original atrioventricular opening is divided into two atrioventricular openings by the formation of the cushion septum, the atrioventricular or cuspid valves are formed in the two atrioventricular openings. These valves prevent the backflow of blood into the atria from the ventricles. At the opening of the sinus into the right atrium, the right and left sides of the opening enlarge and produce folds which project inward into the atrium. These folds form the sinu-atrial (sinu-auricular) valves. During the last week of incubation, a third valve, the Eustachian valve or sinus septum, arises as a fold from the dorsal aspect of the sinus which projects into the right atrium between the openings of the vena cava inferior and the right and left venae cavae superior (precavac). It divides the sinu-atrial opening.

As hatching time approaches, the sinus becomes incorporated almost completely into the walls of the right atrium. A small portion of the sinus probably is incorporated into the cardiac end of the left precaval vein. The sinu-atrial valves also disappear and the fenestrae of the atrial septum gradually close.

b) Mammalian Heart: 1) Early Features. The early development of the mammalian heart (fig. 339) follows the general pattern of the developing heart of lower vertebrates. A primitive tubular heart composed of a sinus venosus, atrium, ventricle and bulbus cordis is evolved. This simple tubular heart is followed by a typical sigmoid-shaped structure in which the two atrial lobes hang ventrally, one on cither side of the bulbus cordis, while the ventricular region projects caudo-ventrally (fig. 339N). The sinus venosus is much smaller, relatively speaking, than that formed in lower vertebrates and tends to be placed toward the right side of the heart in relation to the future right atrium. By the fifth and sixth weeks in the human (fig. 3390), the heart attains outwardly the general appearance of the four-chambered heart.

2) Internal Partitioning. The internal divisions of the heart begin to appear



in the human at about the fifth week, and in the pig at about 4 mm. or 17 days. This process is similar in the human and the pig, and while the following description pertains particularly to the pig it may be applied readily to the developing human heart. In the pig, as in the chick, a crescentic fold or septum of the atrial chamber begins to grow caudally toward the atrioventricular opening from the antero-dorsal region of the atrium. This septum forms the septum primum or interatrial septum I (fig. 340A). As this septum grows caudad, two thickenings, the endocardial cushions, one dorsal and one ventral, arise in the atrioventricular opening (fig. 340B) . The endocardial cushions fuse and divide the atrioventricular canal into two openings. The septum primum ultimately joins and fuses with the endocardial cushions, but the septum as a whole is incomplete, an interatrial opening being present (fig. 340C). Meanwhile, the sinus venosus shifts more completely toward the right atrium, and the opening of the sinus into the right atrium also shifts dextrally. This permits an enlarged area to appear between the interatrial septum and the valvulae venosae, or valves of the sinus venosus guarding the sinu-atrial opening. In this area, interatrial septum II or septum secundum, arises as a downgrowth from the atrial roof (fig. 340C, D). This second septum eventually produces a condition as shown in figure 340D. The arrow denotes the passageway or foramen ovale in the septum secundum and also the outlet for the blood into the left atrium over the dorsal part of the valve of the foramen ovale (valvula foraminis ovalis), derived from the atrioventricular end of septum I. This condition persists until birth. The valve of the foramen ovale derived from septum 1 prevents the backflow of blood from the left atrium into the right atrium.

The atrioventricular valves are shown also in figure 340D, together with the fibrous attachments of these valves to the muscular columns of the left and right ventricles. The atrioventricular or cuspid valves arise as thickened, shelf-like growths of connective tissue, to which the tendinous cords from the papillary muscles become attached. The left and right ventricles arc produced as in the chick by the upgrowth from the ventricular apex of the interventricular septum. In the human, the interventricular septum fuses with the endocardial cushions during the eighth to ninth weeks. The papillary muscles projecting inward into the ventricular cavities (fig. 340D) represent modifications of the trabeculae carneae (fig. 340B).

J ) Fate of the Sinus Venosus. The developing superior and inferior venae cavae open into the right horn of the sinus venosus. As the right atrium enlarges it absorbs this right horn into its walls and the venae cavae obtain separate openings into the right atrium (fig. 340D). The body of the sinus venosus becomes the coronary sinus which opens into the right atrium below the opening of the inferior vena cava. The coronary veins empty into the coronary sinus. The left horn of the sinus venosus may persist as a part of the oblique vein of the left atrium (fig. 340F).

/. Fate of the Segments of the Early Embryonic Heart in Various Vertebrates

Fishes Amph ibia Reptiles Birds Mammals

Sinus venosus Retained as separate Retained as separate Small and closely Taken up almost Practically the same as chamber of the chamber of the united with right completely within in birds

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4) The Division of the Bulbus Cordis (Truncus Arteriosus and Conus). The division of the bulbus cordis occurs synchronously with the above changes. Two internal ridges opposite each other are formed during this process. These ridges fuse and divide the bulbus in a spiral fashion into a dorsal aortic root and a pulmonary trunk as indicated in figure 340E. The pulmonary trunk opens into the right ventricle, and the aortic root opens into the left ventricle. Three cup-shaped, semilunar (pocket) valves are developed from internal ridges in the areas between the base of the aortic trunk and the left ventricle and between the base of the pulmonary trunk and the conus portion of the right ventricle (fig. 340E).

4. Modifications of the Aortal Arches

When the heart begins to form, its position is ventro-posteriorly to the developing pharyngeal area. As the pharyngeal region enlarges, the heart recedes, relatively speaking, and moves caudally. This caudal recession of the primitive heart in relation to the pharyngeal area is greater in fishes than in the amphibia and higher vertebrates. Therefore, the ventral aortae (and later ventral aorta) are longer in fishes than in other vertebrates. Actually, in the amphibia and particularly in the higher vertebrates, the primitive heart itself tends to lie below the pharyngeal area. Consequently, the bulbus cordis or anterior end of the primitive heart comes to lie below the midpharyngeal region, and the aortal arches in amphibia and in higher vertebrates arise from the anterior end of the primitive heart in bouquet fashion (figs. 34 IE, 342 A, E). On the other hand, in fishes, a single, elongated, ventral aorta is formed, which extends the length of the pharyngeal area. The developing heart is attached to its caudal end, and the aortal arches arise along its extent (fig. 341A).

The aortal arches arc paired vessels which run dorsally through the substance of the visceral arches. Six pairs of these arches are formed generally in the gnathostomous vertebrates, although some of them are transitory structures. The first, second, and fifth pairs of aortal arches are the most transitory in all forms above the fishes.

During development the aortal arches are modified differently in the various vertebrate groups. In fishes, a permanent, branchial mechanism is inserted midway along the branchial visceral arches. The aortal arch of each branchial visceral arch is broken up into an afferent vessel, passing from the ventral aorta to the branchial (gill) structure, and an efferent vessel, leading from the gill mechanism to the dorsal aorta (fig. 341B). In the majority of amphibia, the first, second, and third branchial aortal arches become involved temporarily in the development of gill mechanisms, although some, such as Necturus, retain the gills permanently. In higher vertebrates, none of the aortal arches are concerned with gill formation, and are, in consequence, transformed directly into the adult form.



The transformation of the aortal arches in the shark, frog, chick, and mammal is shown in figures 341 and 342. It is important to observe that, in those vertebrates possessing lungs, the pulmonary artery grows back from the sixth aortal arch. In a sense, however, the pulmonary arteries represent a direct caudal growth from the posterior ventral aortae, particularly in reptiles, birds, and mammals (fig. 342 A, B, C, E, F, G).

5. Dorsal Aortae (Aorta) and Branches

Two dorsal aortae arise first, one on either side of the notochord and above the primitive gut tube, and their origin is synchronous with the formation of the ventral, vitelline (subintcstinal ) blood vessels and the heart. Posterior to the pharyngeal area, the primitive dorsal aortae soon fuse to form a secondary vessel, the dorsal aorta, lying below the notochord. Anteriorly, in the pharyngeal area, they remain separate, and the cephalic end of each primitive dorsal aorta grows forward into the developing forebrain area. These forward growths of the primitive dorsal aortae into the forebrain area form the anterior rudiments of the internal carotid arteries. The primitive dorsal aortae, therefore, give origin to a single secondary vessel, the dorsal aorta, which is bifurcated at its cephalic end in the region of the pharyngeal area of the gut.

Aside from the cephalic ends of the internal carotid arteries, three main sets of arteries arise from the developing dorsal aorta:

1 ) Dorsal intersegmental arteries, passing between the somites and sending a dorsal branch toward the neural tube and epaxial musculature and a lateral branch into the hypaxial musculature (fig. 343A). The lateral branches develop into intercostal and lumbar arteries of the

Fig. 341. Modifications of the aortal arches. In the following diagrams, the aortal arches are depicted in such a way as to represent two parts, viz. an afferent system, conveying the blood from the heart to the branchial (gill) region, and an efferent system, leading the blood away from the branchial area. The afferent system of vessels is finely stippled, whereas the efferent system is ringed with lines. With the exception of certain lateral views all diagrams have been made from the dorsal view. ( A-D) Aortal vessel changes in embryos of Squalus acanthias. (A and B, adapted from actual conditions described by Scammon, 1911. See reference under Fig. 339.) (A) Generalized, basic

condition present in embryo of 15 mm. embryo. (B) Lateral view, 20.6 mm. stage. (C and D) The afferent and efferent systems in the adult form. D should be superimposed upon C. Diagrams C and D have been separated to minimize confusion. (E-G) Modifications of the aortal arches in the frog. The modifications of the aortal arches in the frog involve a complicated series of changes. In Fig. 335 (A) the simple tubular aortal arches are shown during the earlier phases of development. In Fig. 257 (B) a later stage is depicted. In the latter figure the aortal arches are separated into functional afferent and efferent vessels supplying the branchiae or gills. At the time of metamorphosis the vessels are reorganized, apparently, into tubular vessels according to the pattern shown in Fig. 341 (E). The transformations of the basic conditions shown in Fig. 341 (E) into the adult form are outlined in Figs. 341 (F and G). (H) The

three divisions of the bulbus cordis in the turtle.






Fig. 341. (See facing page for legend.)



adult. The arteries to the bilateral appendages arise as modifications of the lateral branches of the intersegmental arteries (fig. 343B, C').

2) Lateral arteries which are not as truly segmented as are the dorsal intersegmental arteries. They pass laterally into the developing nephrotomic structures (fig. 343A). The renal and genital arteries of the adult are derived from the lateral series of arteries.

3) Ventral arteries much fewer in number than the above-mentioned series (fig. 343A). The vitelline arteries of the yolk-sac area are the first of these ventral arteries to develop. In the Amniota, the umbilical or allantoic arteries also belong to the ventral series of arteries arising from the dorsal aorta. These vessels pass to the placenta or allantoic areas. The coeliac, superior mesenteric, inferior mesenteric, and umbilical arteries are the adult derivatives of the ventral series of arteries arising from the primitive dorsal aorta.

£. Development of the Lymphatic System

The lymphatic system often is called the white blood circulatory system because red blood cells are not present normally, its blood being composed of a lymph fluid and various types of white blood cells.

Lymph vessels are present in all gnathostomous vertebrates, particularly in the bony fishes and in amphibia, reptiles, birds, and mammals. They appear to be absent in cyclostomes. The lymphatic system is highly developed in the amphibia where it possesses lymph hearts, which actively propel the lymphatic fluid forward. Lymph hearts are found in the tail region of bird embryos, including the chick. However, lymph flow on the whole is of a sluggish nature. Lymph vessels never join arteries but connect in various regions with the veins. In larval amphibia and in certain adult species of amphibia, these connections with the venous system may be numerous.

Fig. 342. Modifications of the aortal arches (Continued). (A) Generalized, basic condition of the aortal arches in the chick embryo developed during the first 314 days of incubation. (B) Left lateral view of condition present during latter part of the third day. (C) Schematic representation of changes in aortal arches, dorsal aortae, and the aortal sac of the chick embryo after the first week and a half of incubation. Observe that each external carotid artery arises from the anterior end of a ventral aortic root plus an anastomosis with the common carotid segment. Note further that the right and left sixth aoral arches persist until approximately the twenty-first day (see diagram D). (Diagram C is based to some extent upon data supplied by Pohlman, 1920 . Anat. Rec. 18 .) (D) Dorsal view of adult condition of aortal-arch and bulbus cordis derivatives in the developing chick after hatching. (E) Generalized aortal arch condition in mammalian embryo. (F) Dorsal view of aortal arches of about 6 mm. human embryo. (G) Lateral view of same. (This figure redrawn and adapted from Patten, 1946 . Human Embryology, Blakiston, Philadelphia, after Congdon.) (H) Dorsal view of aortal arches of 14 mm. embryo. (I) Left lateral view of same. (This figure is redrawn and adapted from Patten, 1946 . Human Embryology, Blakiston, Philadelphia.) (J) Dorsal view of conditions present after birth. (See also Fig. 379.)


Fig. 342. (See facing page for legend.)




Two general views are held as to the origin of the lymphatic system. One view holds that lymphatic vessels develop independently of blood vessels and originate as small spaces in the mesenchyme, the mesenchymal cells flattening and forming an endothelial lining for the space (Huntington, T4). Such primitive lymph spaces fuse with nearby lymph spaces to form discrete channels (McClure, ’21). A second view maintains that the certain, small lymph sacs arise from small endothelially lined channels which are a part of the primitive venous plexuses in certain areas (Sabin, ’12, p. 709). Both views agree, however, that once formed, the primitive lymph vessels grow and spread by sprouting new channels from previously established vessels (Clark and Clark, ’32).

The first lymphatic capillaries appear to develop along the main veins. In certain regions, these capillaries give origin to the lymph sacs. Right and left jugular lymph sacs arise in the mammal along the anterior cardinal veins at the base of the neck (fig. 343D). These lymph sacs grow, expand, and coalesce with smaller adjoining lymph spaces. Various other lymph sacs arise, such as the subclavian lymph sac which is associated with the subclavian vein in the axillary region, the cisterna chyli which arises from the retroperitoneal, median lymph sac in the lumbar area, and the iliac lymph sacs which arise posterior to the retroperitoneal rudiment of the cisterna chyli. From these central lymph sacs, the peripheral lymph channels arise and grow rapidly in a distal direction. The thoracic duct comes into existence as a longitudinal vessel along the middorsal area of the body and together with the left jugular lymphatic trunk opens into the venous system near the junction of the internal and external jugular veins. The right jugular lymphatic trunk opens into the venous system similarly on the right side. From these main lymphatic areas, smaller peripheral channels arise as endothelial outgrowths. Valves develop within.

Fig. 343. Branches of dorsal aorta; lymphatic structures. (A) Diagram illustrating various branches of dorsal aorta. (B) Arteries of brain area, appendages, body wall and umbilical cord of human embryo of seven weeks. (Redrawn from Patten, 1946. Human Embryology, Blakiston, Philadelphia, after Mall.) (C and C') Two stages in development of forelimb arteries of pig: C, embryo of 4.5 mm.; C', embryo of 12 mm. (Redrawn from Woollard, 1922. Carnegie Contribution to Embryology, No. 70, Vol. 14.) (D) Formation of primitive lymph sacs in the mammal (cat). (Redrawn from

F. T. Lewis, 1906. Am. J. Anat. 5.) (E and E') Four stages in the development of a lymph node. (Redrawn from Bremer, 1936. A Text-book of Histology, Blakiston, Philadelphia.) Diagram E, to the left. Lymphatic vessels come to surround a mass of primitive lymphoid tissue composed of mesenchymal tissue and lymphocytes. Primitive connective tissue surrounds the mass. Diagram E, to the right. The ingrowing lymphatic channels break up the lymphoidal tissue with the subsequent formation of lymph sinuses. Observe that a peripheral lymph channel is established, and also that the surrounding connective tissue is beginning to form a surrounding capsule from which trabeculae are growing into the lymphoidal mass. Diagram E', to the left. Further development of growth changes shown in E, to the right. Diagram E', to the right. A loose meshwork of lymph channels and sinuses appears in the central portion or medulla of the lymph node, whereas the periphery or cortex is composed of secondary nodules separated into compartments by the ingrowth of trabeculae from the peripheral capsule.












Fig. 343. (See facing page for legend.)




A characteristic feature of the lymphatic system is the development of lymph nodes (lymph glands) along the lymphatic vessels. A lymph node is a small, rounded structure with lymph vessels entering it at various points (fig. 343E). From these lymph vessels, a flow of lymph oozes around a meshwork of lymphoid cords, contained within the lymph node. After passing through the meandering lymph spaces within the node, the lymph emerges from the opposite side of the lymph node into lymphatic channels.

Lymph nodes appear to arise from lymph sacs which are invaded by ingrowing mesenchyme and connective tissue. Lymphoblasts become associated with these connective-tissue ingrowths, and lymphocytes are differentiated in large numbers. Eventually the developing lymph node forms two areas, an outer cortex, containing dense masses of lymphocytes and an inner medulla, containing a loose meshwork of lymph channels and sinuses. Connective tissue forms a capsule around the lymph node from which partitions or trabeculae grow inward to divide the cortex into secondary nodules. Beneath the capsule, a peripheral lymph sinus is developed. Blood vessels enter the lymph node at the hilus and pass along the trabeculae to the secondary nodules. The returning blood vessels follow the same pathways.

The spleen is a large lymph gland attached to the omental derivative of the dorsal mesogastrium or peritoneal support of the stomach. It arises as a concentration of mesenchyme along the left aspect of the early mesogastrium. This mesenchymal mass eventually increases in size and projects from the surface of the mesogastrium from which it later becomes suspended by a constricted peritoneal support, the gastro-splenic ligament.

The mesenchymal mass of the developing spleen is well supplied with blood vessels, and a completely closed set of vascular channels is formed at first. Later, however, sinus-like spaces appear which unite with the closed vascular channels converting the closed system into one possessing open sinuses. Lymphoid tissue forms and masses of splenic corpuscles develop about the blood vessels. (Consult Maximow and Bloom, ’42, for detailed description of splenic structure.)

F. Modifications of the Circulatory System in the Mammalian Fetus

at Birth

Consult Chap. 22.

G. The Initiation of the Heart Beat

The first parts of the heart to be developed are the anterior regions, namely, the bulbus cordis and the ventricle. When the ventricular region is developed in the chick, it starts to twitch. Later when the atrial portion is formed, it commences to contract with a rhythm different from that of the ventricular area, and its beat supersedes that of the ventricle. Still later when the sinus venosus is established, it emerges with its own contraction rhythm, and this



rhythm then dominates the contraction wave which spreads forward over the heart. The area of the sinus continues to be the “pacesetter” of the heart beat throughout life, although in birds and mammals, the sinus is taken up into the posterior wall of the right atrium. In the mammal (fig. 340F), the sinus node, located in the right atrium, initiates, under normal conditions, each heart beat. The contraction stimulus spreads distally to the peculiar fibrous bundle, located in the atrial septum and the atrioventricular area. This bundle is known as the atrioventricular node, and its fibers descend into the muscles of the ventricular area, conveying the heart beat to the ventricles.

Though fibers from the autonomic nervous system reach the heart in the region of the right atrium and stimuli from these nerves may greatly affect the rhythm of the heart beat, the essential control of the beat lies within the heart’s own nodal system (fig. 340F).


Bloom, W. and Bartelmez, G. W. 1940. Hematopoiesis in young human embryos. Am. J. Anat. 67:21.

Clark, E. R. and Clark, E. L. 1932. Am. J. Anat. 51:49.

Gilmour, J. R. 1941. Normal haemopoiesis in intra-uterine and neonatal life. J. Path. & Bact. 52:25.

Hochstetter, F. 1906. Chap. IV in Handbuch der vergleichenden und experimentellen Entwickelungslehrc der Wirbeltiere by O. Hertwig. Gustav Fischer, Jena.

Huntington, G. S. 1914. Development of lymphatic system in amniotcs. Am. J. Anat. 16:127.

Jordan, H. E. and Speidel, C. C. 1923a. Blood cell formation and destruction in relation to the mechanism of thyroid accelerated metamorphoses in the larval frog. J. Exper. Med. 38:529.

and . 1923b. Studies on

lymphocytes. I. Effects of splenectomy, experimental hemorrhage and a hemolytic toxin in the frog. Am. J. Anat. 32:155.

Kampmeier, O. E. 1920. The changes of the systemic venous plan during development and the relation of the lymph hearts to them in Anura. Anat. Rec. 19:83.

Maximow, A. A. and Bloom, W. 1942. A Textbook of Histology. Saunders, Philadelphia.

McClure, C. F. W. 1921. The endothelial problem. Anat. Rec. 22:219.

Miller, A. M. 1903. The development of the postcaval vein in birds. Am. J. Anat. 2:283.

Minot, C. S. 1912. Chap. 18, Vol. II, p. 498, The origin of the angioblast and the development of the blood in Human Embryology by Keibel, F. and Mall, F. P. J. B. Lippincott Co., Philadelphia.

Noble, G. K. 1931. The Biology of the Amphibia. McGraw-Hill, New York and London.

Reagan, F. P. 1917. Experimental studies on the origin of vascular endothelium and of erythrocytes. Am. J. Anat. 21:39.

Sabin, F. R. 1912. Chap. 18, Vol. II, p. 709, Development of the lymphatic system in human embryology by Keibel, F. and Mall, F. P. J. B. Lippincott Co., Philadelphia.

Scammon, R. E. 1913. The development of the elasmobranch liver. Am. J. Anat. 14:333.

Stockard, C. R. 1915. The origin of blood and vascular endothelium in embryos without a circulation of the blood and in normal embryos. Am. J. Anat. 18:227.

Cite this page: Hill, M.A. (2021, January 27) Embryology Book - Comparative Embryology of the Vertebrates 4-17. Retrieved from

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