Paper - The development of the sympathetic system in birds (1910)

From Embryology
Embryology - 15 Jul 2020    Facebook link Pinterest link Twitter link  Expand to Translate  
Google Translate - select your language from the list shown below (this will open a new external page)

العربية | català | 中文 | 中國傳統的 | français | Deutsche | עִברִית | हिंदी | bahasa Indonesia | italiano | 日本語 | 한국어 | မြန်မာ | Pilipino | Polskie | português | ਪੰਜਾਬੀ ਦੇ | Română | русский | Español | Swahili | Svensk | ไทย | Türkçe | اردو | ייִדיש | Tiếng Việt    These external translations are automated and may not be accurate. (More? About Translations)

A personal message from Dr Mark Hill (May 2020)  
Mark Hill.jpg
I have decided to take early retirement in September 2020. During the many years online I have received wonderful feedback from many readers, researchers and students interested in human embryology. I especially thank my research collaborators and contributors to the site. The good news is Embryology will remain online and I will continue my association with UNSW Australia. I look forward to updating and including the many exciting new discoveries in Embryology!

Kuntz A. The development of the sympathetic system in birds. (1910) J Comp. Neurol. 20: 211-258.

Online Editor  
Mark Hill.jpg
This historic 1910 paper by Kuntz describes the development of the sympathetic nervous system in mammals.



Also by this author: Kuntz A. A contribution to the histogenesis of the sympathetic nervous system. (1909) Anat. Rec. 3,: 458-465.

Kuntz A. The role of the vagi in the development of the sympathetic nervous system. (1909) Anat. Anz. 35: 381-390.

Kuntz A. The development of the sympathetic nervous system in mammals. (1910) J Comp. Neurol. 20: 211-258.

Kuntz A. The development of the sympathetic system in birds. (1910) J Comp. Neurol. 20: 211-258.

Kuntz A. The development of the sympathetic nervous system in man. (1920) J. Comp. Neurol. 32(2): 173-229.

Modern Notes: peripheral nervous system

Neural Crest Links: neural crest | Lecture - Early Neural | Lecture - Neural Crest Development | Lecture Movie | Schwann cell | adrenal | melanocyte | peripheral nervous system | enteric nervous system | cornea | cranial nerve neural crest | head | skull | cardiac neural crest | Nicole Le Douarin | Neural Crest Movies | neural crest abnormalities | Category:Neural Crest
Historic Embryology - Neural Crest  
1879 Olfactory Organ | 1905 Cranial and Spinal Nerves | 1908 10 mm Peripheral | 1910 Mammal Sympathetic | 1920 Human Sympathetic | 1939 10 Somite Embryo | 1942 Origin | 1957 Adrenal


Neural Links: ectoderm | neural | neural crest | ventricular | sensory | Stage 22 | gliogenesis | neural fetal | Medicine Lecture - Neural | Lecture - Ectoderm | Lecture - Neural Crest | Lab - Early Neural | neural abnormalities | folic acid | iodine deficiency | Fetal Alcohol Syndrome | neural postnatal | neural examination | Histology | Historic Neural | Category:Neural


Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

The Development of the Sympathetic Nervous System in Birds

Albert Kuntz
Albert Kuntz (1879–1957)

Albert Kuntz

From the Biological Laboratory, State University of Iowa

Ten Figures

  • From the Laboratories of Animal Biology of the State University of Iowa. Prof. Gilbert L. Houser, Director.

Introduction

The present investigation of the development of the sympathetic nervous system in birds has grown out of an investigation of the development of the sympathetic nervous system in mammals. It was undertaken in order to further exact knowledge concerning the development of the sympathetic nervous system, to extend the writer's observations on the histogenesis of the sympathetic nervous system in mammals, and to point out certain morphogenetic differences in the development of the sympathetic system in birds and in mammals, with a view to their phylogenetic significance.

Birds and mammals have become specialized along divergent lines. Their special habits of life have brought about modification in the course of ontogeny as well as in adult structure. The sympathetic nervous system, which is concerned primarily with the control of the purely vegetati\e functions, has not escaped the modifying influence of specialized habits. It is hoped, therefore, that a more exact knowledge of the development of the sympathetic nervous system in birds may throw some new light on the problems involving the structural and the functional relationships of the sympathetic system to the central nervous system.

Inasmuch as the literature bearing on the development of the sympathetic nervous system has been reviewed by the writer in a recent paper, only such references will be made to the literature in this paper as seem to be necessary.

The observations set forth in the following pages are based on embryos of the chick. The embryos were fixed in chrom-acetoformaldehyde. The sections were cut to a thickness of 10 micra and stained by the iron-haematoxylin method. This method, as indicated in the earlier paper, was found best adapted for purposes of this research.

Observations

1. Sympathetic trunks

(a.) Introductory

His, Jr. ('97) called attention to the fact that in the chick two pairs of sympathetic trunks arise in the course of ontogeny. These he has designated as the "primary" and the ' ' secondary ' ' sympathetic trunks. According to his observations, the primary sympathetic trunks arise about the close of the third day of incubation, as a pair of cell-columns lying along the sides of the dorsal surface of the aorta. About the beginning of the sixth day, the anlagen of the secondary sympathetic trunks arise as cell-aggregates situated just median to the ventral roots of the spinal nerves. These cell-aggregates are at first independent of each other, but become united later by longitudinal commissures. Between the fourth and the eighth day of incubation, the primary sympathetic trunks disappear, except in the most anterior region, becoming resolved into the ganglia and nerves constituting the prevertebral and the peripheral sympathetic plexuses. According to His, Jr., the cells giving rise to both the primary and the secondary sympathetic trunks are derived exclusively from the spinal ganglia.



Fig. 1. Diagramatic transverse section through the thoracic region of an embryo of the chick (130 hours incubation), ao., aorta; nc., notochord; p.sy., primary sympathetic trunks; sp.g., spinal ganghon; sp.n., spinal nerve; s.sy., secondary sympathetic trunks.


My observations on the development of the sympathetic trunks in the chick do not differ essentially from those of His, Jr., except in one particular. I find that the cells giving rise to the primary and the secondary sympathetic trunks in the chick, like the cells giving rise to the sympathetic trunks in mammals, are not derived exclusively from the spinal ganglia, as His, Jr., believes them to be, but that they have their origin, wholly or in part, in the neural tube.


Figure 1 has been introduced to show the relative positions of the primary and the secondary sympathetic trunks in an embryo of the chick in the 130- hour stage.

(b.) Primary sympathetic trunks

The primary sympathetic trunks arise about the beginning of the fourth day of incubation, as cell-aggregates lying along the sides of the aorta and along the dorsal surfaces of the carotid arteries. At the close of the fourth day (96- hour stage) , these cell-aggregates have assumed the appearance of loosely aggregated cell-columns (fig. 2, A, p. sy.). Well marked ganglionic enlargements do not occur, but the cell-columns are not of uniform diameter. In the posterior region, the anlagen of the primary sympathetic trunks arise a little later than in the anterior region, and remain less sharply limited. They are, at this stage, not directly connected with the spinal nerves. In the thoracic region where the spinal nerves are best developed, they extend peripherally a little beyond the level of the aorta. At a point a little above the level of the aorta, cells deviate from the course of the spinal nerves and wander through the mesenchyme, either singly or in small groups, toward the sides of the aorta (fig. 2, A and B, i. c. c. r.) where they become aggregated to give rise to the anlagen of the primary sympathetic trunks.

During the course of the fifth day of incubation, the primary sympathetic trunks become more conspicuous. They move dorsally and recede a short distance from the walls of the aorta until at the close of the fifth day (120-hour stage) they appear as conspicuous cell-columns lying along the dorso-lateral aspects of the aorta a short distance from its surface (fig. 2, C, p. sy.). The primary sympathetic trunks are now sharply defined in the anterior region and are connected with the spinal nerves by distinct cellular tracts. In the posterior region, the cell-aggregates are still loosely scattered along the sides of the aorta and the cellular tracts connecting them with the spinal nerves are less distinct. The primary sympathetic trunks have now reached their maximum development. During the course of the sixth day, they decrease materially in size until at the close of the sixth day (144hour-stage) they have almost disappeared. Their complete disappearance occurs first in the thoracic region, while the last remnants may be observed in the anterior cervical region.

(c.) Secondary sy?npathetic trunks

The anlagen of the secon dary sympathetic trunks arise about the beginning of the sixth day (120-hour stage), as ganglionic enlargements on the median sides of the spinal nerves at the point of origin of the communicating rami (fig. 2, C, s. sy.). These ganglionic enlargements are at first independent of each other, but become united later by longitudinal commissures. Like the anlagen of the primary sympathetic trunks, the anlagen of the secondary sympathetic trunks appear earliest in the thoracic region and latest in the sacral region. At the beginning of the sixth day there are as yet no traces of the anlagen of the secondary sympathetic trunks in the posterior half of the body. During the course of the sixth day, the secondary sympathetic trunks become larger and more conspicuous, while the primary sympathetic trunks become correspondingly smaller. The former, being located at the point of origin of the communicating rami, are connected with the latter by the cellular tracts which connect them with the spinal nerves (fig. 2, C).



Fig. 2. Transverse sections showing successive stages in the development of the primary and the secondary sympathetic trunks in the chick. A., primary sympathetic trunk (96 hours incubation), X 200. B., Primary sympathetic trunk (105 hours incubation), X 200. C, Primary and secondary sympathetic trunks (120 hours incubation), X 200. D., Secondary sympathetic trunk (144 hours incubation), X 100. ao., aorta; c.r., communicating ramus; i.c.c.r., cells migrating from spinal nerve to primary sympathetic trunk; i.c.n., indifferent cell undergoing mitosis; p.sy., primary sympathetic trunk; sp.n., spinal nerve; s.sy., secondary sympathetic trunk.



As the communicating rami become fibrous, the anlagen of the secondary sympathetic trunks become removed a short distance from the spinal nerves. In the cervical and the thoracic region they are removed to the ends of the short communicating rami (fig. 2, D, s. sy.). In the posterior region of the body, the fibers of the communicating rami extend beyond the anlagen of the secondary sympathetic trunks. At the close of the sixth day, they may be traced through the cell-aggregates still remaining scattered along the sides of the aorta, into the anlagen of the prevertebral plexuses.

In the posterior region of the body, the distinction between the primary and the secondary sympathetic trunks is never well marked. Cells gradually become aggregated in the proximal part of the communicating rami to give rise to the secondary sympathetic trunks, while the cells constituting the primary sympathetic trunks migrate ventrally into the anlagen of the prevertebral plexuses. After the sixth day, the secondary sympathetic trunks become more distinct throughout their entire length, as the ganglionic enlargements become connected by the fibers of the longitudinal commissures.

(d.) Histogenesis

As already indicated, the sympathetic trunks arise from cells which migrate peripherally from the cerebrospinal nervous system along the spinal nerves. As soon as fibers appear in the ventral roots of the spinal nerves (72-hour stage) cells may be traced from the motor niduli, across the marginal veil, into the proximal part of the ventral nerve-roots. Medullary cells become aggregated in the proximal part of the ventral nerve-roots and soon appear to migrate peripherally along the nerve-fibers. While the spinal ganglia are becoming differentiated from the neural crest, cells apparently having their origin in the neural tube wander out into the spinal ganglia. Evidence of this process may be observed as early as the 64-hour stage. During the fourth and the fifth day, after the spinal ganglia have become well differentiated, a few cells may be observed migrating from the dorsal part of the neural tube into the dorsal nerveroots (fig. 3, c. m. d. n. r.). It is probable that cells do not migrate from the dorsal part of the neural tube in any considerable numbers after the spinal ganglia have become differentiated. Cell migration into the dorsal nerve-roots is probably only a transient process which takes part in the development of the spinal ganglia.



Fig. 3. Transverse section of the neural tube and the spinal ganglion of an embryo of the chick (105 hours incubation), X 190. c.m.d.n.r., cells migrating into dorsal nerve-root; c.m.v.r., cells migrating into ventral nerve-root; g.c, germinal cells of His; m.n.r., motor nerve-root; nc, notochord; sn.r., sensory nerve-root; sp.g., spinal ganglion; sp.n., spinal nerve.



As the cells in the ventral nerve-roots migrate peripherally, they mingle with similar cells which wander down from the spinal ganglia. As there is no recognizable difference between the cells which wander out from the spinal ganglia and those which migrate peripherally along the ventral nerve-roots, it is impossible to distinguish between the cells from these two sources after they have passed beyond the point of union of the sensory and the motor nerve-roots. As these cells migrate peripherally along the spinal nerve-trunks, some of them deviate from the course of the spinal nerves and migrate toward the sides of the aorta where they become aggregated to give rise to the primary sympathetic trunks. As migration proceeds, the cells which deviate from the course of the spinal nerves no longer migrate into the primary sympathetic trunks, but become aggregated at the median sides of the spinal nerves to form the ganglionic enlargements which constitute the anlagen of the secondary or permanent sympathetic trunks.

His, Jr., has expressed the opinion that the elements composing the primary sympathetic trunks are resolved into the ganglia and nerves of the prevertebral and the peripheral sjmipathetic plexuses. In view of the comparatively enormous development of the prevertebral plexuses and of the ganglion of Remak in birds, this is obviously the fate of the elements composing the primary sympathetic trunks in the posterior region of the body. There is no evidence, however, of the peripheral migration of cells from the primary sympathetic trunks in the anterior region. While there may be some migration posteriorly along the primary sympathetic trunks, it is more probable that most of the elements composing these trunks in the anterior region of the body are withdrawn into the anlagen of the secondary or permanent sympathetic trunks along the cellular tracts connecting the former with the latter. The last remnants of the primary sympathetic trunks in the anterior cervical region, as His, Jr., has suggested, probably atrophy.

The period of incubation being comparatively shorter in birds than in mammals, cell migration takes place much more rapidly. It is at its height in the chick during the fourth and the fifth day of incubation. During this time breaches occur frequently in the external limiting membrane of the neural tube just opposite the motor niduli, and medullary cells may be traced without difficulty from the motor niduli into the proximal part of the ventral nerve-roots (fig. 3, c. m. v. r.). Numerous accompanying cells are present in the spinal nerve-trunks as far as the latter may be traced. At the close of the sixth day, the number of cells present in the spinal nerves has materially decreased. While cells are still moving peripherally along the spinal nerves, it is probable that migration from the neural tube and the spinal ganglia has practically ceased.



Fig. 4. Neuroblasts drawn with the aid of the camera lucida, X 825. a., in ventral nerve-root inside external limiting membrane (105 hours incubation); b., in ventral nerve-root outside external limiting membrane (105 hours incubation); c, in spinal nerve (105 hours incubation); t/., in communicating ramus (105 hours incubation); e., in ventral nerve-root (96 hours incubation): /., in spinal nerve (96 hours incubation).


The great majority of the cells migrating peripherally along the spinal nerves are characterized b} r very little cytoplasm, and by large rounded or elongated nuclei usually having their chromatin aggregated into one or two dense masses. These are obviously the " indifferent " cells of Schaper. Among these are found a few cells which are characterized by large rounded or elongated nuclei showing one or two dense masses of chromatin, and a larger cytoplasmic body which is usually drawn out to a point at one side. Fig. 4 shows several of these cells drawn with the aid of the camera lucida. These are obviously the " neuroblasts" of Schaper. The majority of the cells present in the mantle layer in the neural tube answer to the descriptions given above for the two types of cells migrating peripherally along the spinal nerves. There can be no doubt, therefore, that the cells accompanying the fibers of the spinal nerves have the same histogenetic relationships as the cells which give rise to the neurones and the neuroglia cells in the central nervous system. They are all the descendants of the "germinal" cells (Keimzellen) of His.

These observations are in full accord with the writer's observations on mammalian embryos. There is a marked difference, however, in the chromatin structure of the embryonic medullary cells in birds and in mammals. In mammalian embryos, the migrant medullary cells are usually quite readily recognized by the chromatin structure of their nuclei. They also usually take a slightly deeper stain than the cells of the surrounding mesenchyme. In birds, the chromatin structure of the embryonic medullary cells differs very little from the chromatin structure of the typical mesenchyme cells. Nor are they as distinctly separated from the cells of the surrounding mesenchyme by differential stains as is the case in mammals. Although the difficulties in technique are greater in the chick than in mammalian embryos, there can be no doubt that the cells accompanying the fibers of the spinal nerves are migrant medullary cells. Such cells wander out of the neural tube into the ventral nerve-roots in considerable numbers. The number of cells present in the proximal part of the spinal nerves increases rapidly until the maximum rate of migration is reached, and then decreases rapidly until migration ceases, when only a comparative 1 }' small, but fairly constant, number of cells remain distributed along the nerve-fibers. Furthermore, a few of the cells present in the spinal nerves are obviously neuroblasts. Such cells have frequently been observed outside the neural tube and the spinal ganglia. Cajal ('08) described cells which he recognized as nerve cells in the bipolar phase, in the motor roots of the spinal nerves and in certain of the cranial nerves in the chick. These cells, he believes, correspond to the real motor cells in the neural tube. Mitotic figures occur occasionally all along the course of migration and in the sympathetic anlagen. We are not to suppose, therefore, that all the cells taking part in the development of the sympathetic trunks actually migrate as such from their sources in the cerebro-spinal nervous system. Doubtless, many arise by the mitotic division of " indifferent " cells along the course of migration.

2. Prevertebral plexuses

The prevertebral plexuses are derived directly from the primary sympathetic trunks. They arise about the middle of the fourth day (108-hour stage), as cell-aggregates lying along the ventro-lateral aspects of the aorta from the suprarenal bodies posteriorly. In this region the primary sympathetic trunks are not sharply limited ventrally. Sympathetic cells may be traced from the latter directly into the anlagen of the prevertebral plexuses. In the sacral region, the aorta is soon completely surrounded ventrally by a ring of loosely aggregated sympathetic cells (fig. 5, hyp.).

The cell-aggregates constituting the anlagen of the prevertebral plexuses increase very rapidly. At the close of the fourth day (120-hour stage), these plexuses have become well established. Distinct lines of cells may be traced from the primary sympathetic trunks directly into cell-aggregates of considerable size lying along the median sides of the suprarenals, and wandering sympathetic cells may be observed all along the sides of the aorta from the suprarenals posteriorly. The limits of the anlagen of the several prevertebral plexuses cannot be determined at this stage. Traces of one or the other of these plexuses are not wanting in any transverse section in this entire region.


As incubation proceeds, the prevertebral plexuses assume more definite proportions. The cells increase in number and become more closely aggregated. At the close of the sixth day (144-hour stage), nearly all the cells which were present in the primary sympathetic trunks in the posterior region of the body have wandered down into the prevertebral plexuses. Neither cells nor fibers can be traced ventrally from the prevertebral plexuses as yet except in the sacral region. Here numerous cells may be traced from the hypogastric plexus directly into the ganglion of Remak.


Fig. 5. Transverse section through the sacral region of an embryo of the chick (105 hours incubation), X 60. ao., aorta; g.r., ganglion of Remak; hyp., hypogastric plexus; mes., mesentery; nc., notochord; r. rectum; sp.n., spinal nerve.


3. Ganglion of Remak

The ganglion of Remak arises about the middle of the fourth day, .as an oval cell-column lying in the mesentery just dorsal to the rectum (fig. 5, g.r.). Its greatest diameter occurs in the posterior region. It increases in size very rapidly until at the close of the fifth day it has become a large and conspicuous column of closely aggregated cells, with a maximum diameter of about 85 micra (fig. 6, g.r.). Its diameter decreases anteriorly until it terminates in the region of the genital ridges, in a slender cellular cord which Remak has called the intestinal nerve (Darmnerv).



Fig. 6. Transverse section of an embryo through the sacral region of an embryo of the chick (130 hours incubation), X 110. ao., aorta; g.r., ganglion of Remak; hyp., hypogastric plexus; mes., mesentery; r., rectum; sp.n. spinal nerve.


This ganglion was described by Onodi ('86) and by His, Jr. ('97), but, as far as I have been able to learn, no worker before me has traced the cells composing it to their source. My preparations show conclusively that the cells giving rise to the ganglion of Remak are derived directly from the anlagen of the hypogastric plexus. In transverse sections through the posterior sacral region, where the mesentery is broad and the rectum lies close to the anlagen of the hypogastric plexus, cells may be traced from the latter directly into the ganglion of Remak (figs. 5 and 6).

The ganglion of Remak has no counterpart in mammals. It may be of interest to note at this point that an examination of several embryos of the turtle (kindly placed at nry disposal by Dr. F. A. Stromsten, of these laboratories) has shown that while there is no well defined ganglion in this type, corresponding to the ganglion of Remak, there are numerous cell-aggregates associated with the rectum, which evidently constitute the prototype of Remak's ganglion. It is probable, therefore, that this ganglion, so enormously developed in birds, is correlated with oviparous habits.

4. Vagal sympathetic plexuses

(a.) Introductory

In an earlier paper I have shown that in mammals the sympathetic plexuses related to the vagi; viz., the cardiac plexus and the sympathetic plexuses in the walls of the visceral organs, have their origin in cells which migrate from the vagus ganglia and the walls of the hind-brain along the fibers of the vagi. I have, therefore, designated these plexuses as the " vagal sympathetic" plexuses. My observations on embryos of the chick show clearly that in birds also these plexuses have their origin in cells which migrate from the hind-brain and the vagus ganglia.

(b.) Myenteric and submucous plexuses

In embryos of the chick in the 130-hour stage, the vagus trunks may be traced posteriorly along the walls of the oesophagus just a little below its ventral level. The ganglia of the trunk lie close to the walls of the oesophagus just distal to the origin of the trachea. The bifurcation of the trachea occurs farther anteriorly in birds than in mammals, and the bronchi are comparatively longer. Anterior to the bifurcation of the trachea, cells deviate from the course of the vagi along the fibers of their growing branches and wander into the walls of the oesophagus. These cells are so slightly differentiated at this stage that it is no longer possible to trace them after they have entered the denser tissues of the oesophageal walls. Beyond the bifurcation of the trachea, the vagus trunks bend laterally and ventrally round the bronchi and extend along the ventro-lateral aspects of the oesophagus, continually approaching each other posteriorly. At the point where the vagi begin to bend round the bronchi, each vagus trunk gives rise to a slender branch which extends posteriorly along the wall of the oesophagus between the latter and the bronchus. These branches may be traced posteriorly but for a short distance at this stage.

At the close of the sixth day, the vagi have become more conspicuous. In the anterior region, definite lines of cells may be traced from the vagus trunks into the walls of the oesophagus where they become aggregated into more or less distinct groups arranged in two broken rings (fig. 7, m.s.p.). Posterior to the bifurcation of the trachea, cells may be traced dorsally from the vagus trunks into the walls of the oesophagus (fig. 9, m.s.p.). The vagus branches lying between the walls of the oesophagus and the bronchi have become more conspicuous and may be traced posteriorly as far as the region of the lungs. Posterior to the region of the heart, the vagus trunks lie close together and apparently break up to form a plexus ventral to the oesophagus.

During the seventh and the eighth day of incubation, the sympathetic plexuses in the walls of the digestive tube become well established. Branches of the vagi may be traced into the walls of the oesophagus, and the cell-groups constituting the anlagen of the myenteric and the submucous plexuses assume a more definite arrangement.

The sources of the cells giving rise to the myenteric and the submucous plexuses in the walls of the small intestine could not be definitely determined. In the early stages, single sympathetic cells could not be traced in the dense tissues of the walls of the digestive tube. It is difficult, therefore, to determine whether or not such cells migrate posteriorly in the walls of the digestive tube, as is the case in mammalian embryos. It is probable, however, that such is the case. On the other hand, it is probable that some of the cells which take part in the development of the myenteric and the submucous plexuses in the posterior region of the intestine wander out from the ganglion of Remak. There is no evidence of cells entering the sympathetic plexuses in the walls of the digestive tube from the sympathetic trunks or from the prevertebral plexuses, except through the ganglion of Remak, until fibrous connections are established between the former and the latter. There can be little doubt, therefore, that most of the cells taking part in the development of the myenteric and the submucous plexuses in the walls of the small intestine migrate posteriorly from the anlagen of these plexuses in the anterior region of the digestive tube.



Fig. 7. Transverse section through the oesophagus and the vagi of an embryo of the chick (144 hours incubation), X 80. ao., aorta; m.s.p., cells giving rise to myenteric and submucous plexuses; oe., oesophagus; t., trachea; vag.n., vagus trunks.

Fig. 9. Transverse section through the oesophagus and the anlagen of the cardiac plexus of an embryo of the chick (144 hours incubation), X 80. a.c, atrial cavity; a.s., atrial septum; car. p., anlagen of cardiac plexus; m.s.p., cells giving rise to myenteric and submucous plexuses; oe., oesophagus; vag.n., vagus trunks.


(c.) Pulmonary plexuses

In transverse sections through the region of the lungs of embryos in the 144-hour stage, fibers may be traced laterally from the branches of the vagi lying between the oesophagus and the bronchi. Cells wander out along these fibers and become aggregated to give rise to the anlagen of the pulmonary plexuses, (fig. 8, p.p.).




Fig. 8. Transverse section through the region of the lungs of am embryo of the chick (seventh day of incubation), X 80. ao., aorta; oe., oesophagus; p.p., anlagen of pulmonary plexuses; vag. b., branches of the vagi; vag.n., vagus trunks.


(d.) Cardiac plexus

In transverse sections through the region of the head in embryos in the 120-hour stage, cells may be traced ventrally from the vagi into the septum of the atria where they become aggregated into small groups which constitute the anlagen of the cardiac plexus. In later stages, these cell-groups become more conspicuous until at the close of the sixth day they appear as distinct cell-aggregates in the atrial septum (fig. 9, car. p.).


(e.) Histogenesis

In sections through the head-region of embryos in the 96-hour stage, medullary cells may be traced from the walls of the hind-brain into the rootlets of the vagus and the spinal accessory nerves (fig. 10, c.m.vag.r.). That these cells migrate peripherally from the walls of the hind-brain in considerable numbers cannot be doubted. In many sections they may be observed pushing into the nerve-rootlets in cone-shaped heaps as the latter traverse the marginal veil. Occasionally medullary cells are observed half in and half out of the neural tube, and many are present in the nerve-rootlets just outside the external limiting membrane. With similar cells which wander out from the vagus ganglia, these cells migrate peripherally along the fibers of the vagi. As these cells migrate peripherally and the vagi give rise to fibrous branches, cells wander out from the vagus trunks and give rise to the vagal sympathetic plexuses. That such is the origin of the cardiac plexus and the sympathetic plexuses in the walls of the visceral organs in the chick cannot be doubted. The figures of cells migrating from the vagi into the anlagen of these plexuses are perfectly clear. Nor can cells be traced into these plexuses from any other source, except possibly in the posterior region of the intestine, until fibrous connections have been established between the latter and the sympathetic trunks. By this time the great majority of the cells taking part in the development of the vagal sympathetic plexuses are already present. The connections of these plexuses with the sympathetic trunks must, therefore, be looked upon as secondary.


Fig. 10. Transverse section through the wall of the hind-brain of an embryo of the chick (96 hours incubation), X 550. c.m.vag.r., cells migrating into roots of the vagus; el.m,., external limiting membrane; g.c, germinal cells of His; i.l.m., internal limiting membrane; vag.r., roots of vagus nerve.



The period of migration of cells from the hind-brain and from the vagus ganglia along the vagi is coextensive with the period of migration of cells from the neural tube and the spinal ganglia along the spinal nerves. The cells which migrate peripherally along the vagi are cells of the same character as those which migrate peripherally along the spinal nerves; viz., they are the " indifferent" cells and the "neuroblasts" of Schaper. The cells giving rise to the vagal sympathetic plexuses, therefore, have the same histogenetic relationships as those giving rise to the sympathetic trunks. Mitotic figures occur occasionally along the vagi and in the anlagen of the vagal sympathetic plexuses. We are not to suppose, therefore, that all the cells taking part in the development of these plexuses actually migrate as such from their sources in the hind-brain and the vagus ganglia. Doubtless, many arise by the mitotic division of indifferent cells along the course of migration.

Discussion of Results, and Conclusions

The observations set forth in the preceding pages have shown that in birds the sympathetic nervous system has its origin in cells which migrate peripherally from the neural tube and the cerebrospinal ganglia. The cells giving rise to the sympathetic trunks and the prevertebral plexuses, including the ganglion of Remak, migrate peripherally along the spinal nerves, while the cells giving rise to the vagal sympathetic plexuses migrate peripherally along the vagi. These observations agree essentially with the writer's observations on the histogenesis of the sympathetic nervous system in mammals. My observations on the histogenesis of the sympathetic system agree with the findings of Froriep ('07) in embryos of Torpedo and of the rabbit only in regard to the sympathetic trunks and the prevertebral plexuses. Froriep succeeded in tracing medullary cells from the neural tube into the ventral roots of the spinal nerves. According to his observations these cells, with similar cells which wander out from the spinal ganglia, migrate peripherally along the spinal nerves. At the origin of the communicating rami, cells deviate from the courses of the spinal nerves and give rise to the sympathetic nervous system. Inasmuch as Froriep does not admit of the existence of sympathetic sensory neurones, he concludes that all the sympathetic neurones in the sympathetic trunks and the prevertebral and the peripheral sympathetic plexuses arise from cells which have their origin in the ventral half of the neural tube and migrate peripherally along the ventral roots of the spinal nerves. My observations have shown conclusively that the cardiac plexus and the sympathetic plexuses in the walls of the visceral organs do not arise from cells which migrate peripherally along the spinal nerves, but have their origin in cells which migrate from the hindbrain and the vagus ganglia along the vagi. As I have pointed out in an earlier paper, experimental evidence indicates the existence of sympathetic sensory neurones in some of these plexuses. It is probable, therefore, that the sympathetic excitatory neurones arise from cells which migrate from the neural tube along the fibers of the motor nerve-roots, while the sympathetic sensory neurones, wherever such neurones exist, arise from cells which migrate peripherally from the cerebro-spinal ganglia. According to this interpretation, the sympathetic neurones are homologous with the afferent and the efferent components of the other functional divisions of the peripheral nervous system.

Froriep further believes that the axones which constitute the fibers of the motor roots of the spinal nerves are the vehicles by means of which medullary cells are transported peripherally along the spinal nerves, and that cells are carried from the spinal nerves into the anlagen of the sympathetic trunks by the axones which constitute the motor fibers of the communicating rami. He is not convinced as to whether such peripheral transportation is accomplished by the peripheral growth of the axones alone or whether cells may also migrate peripherally, independently of the growth of the axones. My observations do not enable me to offer any adequate explanation of the process by which the cells giving rise to the sympathetic nervous system are carried peripherally from the cerebro-spinal system. The growing nerve-fibers, doubtless, constitute an important factor in the peripheral transportation of these elements. They are not sufficient, however, to account for the entire process alone. Nor is the presence of nerve-fibers absolutely necessary to the peripheral migration of sympathetic cells. In embryos of both birds and mammals, cells may be traced from the spinal nerves into the anlagert of the sympathetic trunks before fibers are present in the communicating rami. Likewise, cells migrate ventrally from the sympathetic trunks into the anlagen of the prevertebral plexuses before postganglionic fibers appear.

Held ('09) and Marcus ('09) have recently taken exception to Froriep's views concerning the origin of the cells giving rise to the sympathetic nervous system. Held has attempted to show, for the entire vertebrate series, that the cells present in the motor nerve-roots play no part in the development of the sympathetic nervous system. He still regards the sympathetic system as an offshoot from the spinal ganglia. In the light of the present investigation, such a position is untenable. My preparations show conclusively that medullary cells migrate into the motor nerveroots in considerable numbers. These cells migrate peripherally along the spinal nerves just as certainly as do the cells which wander down from the spinal ganglia. Inasmuch as the great majority of the cells migrating peripherally along the spinal nerves are cells of an indifferent character, there is no reason to suppose that the cells which wander down from the spinal ganglia give rise to sympathetic neurones, while those which migrate from the neural tube along the fibers of the motor nerve-roots do not.

Marcus has attempted to show that the cells which Froriep observed in the ventral roots of the spinal nerves do not wander out from the neural tube, but migrate thither from the neural crest. In early stages of embryos of torpedo, he has observed cell-chains connecting the neural crest with cell-aggregates in the ventral nerve-roots. He concludes, therefore, that the neural crest represents the sole source of the cells giving rise to sympathetic neurones. I have found no evidence of cells migrating from the neural crest into the ventral roots of the spinal nerves in embryos of birds and mammals. Cell-chains connecting the neural crest with the cell-aggregates in the ventral nerve-roots, doubtless, do occur in embryos of the lower vertebrates. I have observed such cell-chains in embryos of Amblystoma. This does not, however, preclude the possibility of cells migrating from the neural tube directly into the ventral nerve-roots. In the same embryos in which these cell-chains were observed, I was able to trace medullary cells from the ventral part of the neural tube directly into the ventral nerve-roots.

As has already been pointed out, the cells migrating peripherally from the neural tube and the cerebro-spinal ganglia along the spinal nerves and along the vagi are the descendants of the " germinal" cells of His; viz., the "indifferent" cells and the "neuroblasts" of Schaper. They are, therefore, homologous with the cells giving rise to the neurones and the neuroglia cells in the central nervous system. Inasmuch as some of these cells give rise to the sympathetic nervous system, the latter bears a direct genetic relationship to the central nervous system, and the sympathetic neurones are homologous with the afferent and the efferent components of the other functional divisions of the nervous system. The histogenetic relationships of the sympathetic neurones were considered at some length in my paper on the development of the sympathetic nervous system in mammals. They will, therefore, not be considered further at this point.

A comparative study of the morphogenesis of the sympathetic nervous system in birds and in mammals reveals some striking points of difference which evidently have phylogenetic significance. Two pairs of sympathetic trunks arise in the course of ontogeny in birds, while in mammals a single pair of sympathetic trunks is developed. In the early stages in mammalian embryos, the prevertebral plexuses show their maximum development in the region of the suprarenals. In the early stages in the chick, these plexuses show their maximum development in the sacral region. This character in birds is obviously correlated with the enormous development of the ganglion of Remak which has no counterpart in mammals. Minor differences also occur in the development of the vagal sympathetic plexuses. These morphogenetic differences, doubtless, indicate that the sympathetic system has departed more widely from the ancestral type in birds than in mammals.

A study of the development of the sympathetic system in birds, as well as in mammals, warrants the conclusion that the nervous system is a unit of which the sympathetic system is a part homologous with the other functional divisions. It may be looked upon as one of the later accessions to the vertebrate nervous system which has arisen in response to the conditions of the vegetative life. The morphogenetic differences which have been pointed out in the development of the sympathetic system in birds and in mammals obviously indicate specializations in certain directions, which have arisen in response to peculiar vegetative functions.

Summary

  1. The primary sympathetic trunks in the chick arise about the beginning of the fourth day of incubation, as a pair of cellcolumns lying along the sides of the aorta and along the dorsal surfaces of the carotid arteries. The anlagen of the secondary sympathetic trunks arise about the beginning of the sixth day, as ganglionic enlargements on the median sides of the spinal nerves. These ganglionic enlargements are at first independent of each other, but become united later by longitudinal commissures. The primary sympathetic trunks reach their maximum development during the course of the sixth day, after which they decrease in size until they disappear. The observations just summarized agree essential^ with the results of His, Jr.
  2. The author finds, however, that the cells giving rise to the sympathetic trunks are not derived exclusively from the spinal ganglia, as His, Jr., supposes, but that they are derived, wholly or in part, from the neural tube. Medullary cells migrate from the neural tube into the ventral roots of the spinal nerves. With similar cells which wander out from the spinal ganglia, these cells migrate peripherally along the spinal nerves. At a point a little above the level of the aorta, cells deviate from the course of the spinal nerves and, migrating toward the aorta, give rise to the primary sympathetic trunks. As migration proceeds, the cells which deviate from the course of the spinal nerves no longer wander into the primary sympathetic trunks, but become aggregated at the point of origin of the communicating rami and give rise to the anlagen of the secondary sympathetic trunks.
  3. The prevertebral plexuses arise as cell-aggregates lying along the ventro-lateral aspects of the aorta from the suprarenals posteriorly. They are derived directly from the primary sympathetic trunks.
  4. The ganglion of Remak arises as an oval cell-column lying in the mesentery just dorsal to the rectum. It arises from cells which the author finds to migrate ventrally from the hypogastric plexus.
  5. The cardiac plexus and the sympathetic plexuses in the walls of the visceral organs, which the author has designated as the " vagal sympathetic" plexuses in an earlier paper, arise from cells which migrate from the hind-brain and the vagus ganglia along the fibers of the vagi. In the posterior region of the intestine, the myenteric and the submucous plexuses probably receive some cells from the ganglion of Remak.
  6. The cells which migrate from the neural tube and from the cerebro-spinal ganglia along the spinal nerves and the vagi are the descendants of the "germinal" cells of His; viz., the "indifferent" cells and the " neuroblasts" of Schaper. They are, therefore, homologous with the cells which give rise to the neurones and the neuroglia cells in the central nervous system, and the sympathetic neurones are homologous with the afferent and the efferent com ponents of the other functional divisions of the peripheral nervous system. These observations agree with the author's observations on mammalian embryos.
  7. Certain morphogenetic differences exist in the development of the sympathetic nervous system in birds and mammals, which the author interprets as indicating that the sympathetic system has departed more widely from the ancestral type in birds than in mammals. Such departure is no more than should have been expected in the specialized avian branch of the vertebrate series.


Bibliography

Cajal, S. R. Nouvelles observations sur revolution des neuroblastes, avec:

1908. quelque remarques sur l'hypothese neurogenetique de HensenHeld. Anal. Am., vol. 32, pp. 1-25 and 65-78.

Froriep, A. Die Entwickelung und Bau des autonomen Nervensystems. Med. 1907. naturwiss. Archiv., vol. 1, pp. 301-321.

Held, H. Die Entwickelung des Nervensgewebes bei den Wirbeltieren. Leipzig. 1909.

His, Jr., W. Ueber die Entwickelung des Baucksympathicus beira Hiihnchen 1897. und Menschen. Archiv Anat. u. Entwg. Supplement.

Kuntz A. A contribution to the histogenesis of the sympathetic nervous system. (1909) Anat. Rec. 3,: 458-465.

Kuntz A. The role of the vagi in the development of the sympathetic nervous system. (1909) Anat. Anz. 35: 381-390.

Kuntz A. The development of the sympathetic nervous system in mammals. (1910) J Comp. Neurol. 20: 211-258.

1910. A comparative study of the development of the sympathetic nervous system in birds and mammals. Abstract of paper read before the American Society of Zoologists, Central Branch. Science, n.s., vol. 31, p. 837.

Marcus, H. Ueber den Sympathicus. Sitzungsb. d. Gesell. f. Morph. u. Physiol. 1909. in Miinchen, pp. 1-13.

Onodi, A. D. Ueber die Entwickelung des sympathischen Nervensystems. Archiv 1886. /. mikr. Anat., vol. 26, pp. 555-580.

Accepted by the Wistar Institute of Anatomy and Biology, June 10, 1910. Printed, September 14, 1910


Cite this page: Hill, M.A. (2020, July 15) Embryology Paper - The development of the sympathetic system in birds (1910). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_development_of_the_sympathetic_system_in_birds_(1910)

What Links Here?
© Dr Mark Hill 2020, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G