NOTES ON THE DEVELOPMENT OF THE SYMPA

THETIC NERVOUS SYSTEM IN THE

COMMON TOAD.1

By WALTER C. JONES, M.D.

With twelve figures.

The work which forms the basis of this paper was done in 1898-1900, at the Zoological Laboratory of Northwestern University, Evanston, Illinois, and was presented in part fulfillment for the degree of Master of Arts. Circumstances prevented the immediate preparation of the results for publication. In the considerable interval to the present, only one paper, as far as I know, has been published, dealing with the development of the sympathetic nervous system; this paper, by HOFFMANN, 1902, is briefly noticed in my review of the literature. The writer wishes to thank Professor Wм. A. Locy, Director of the Laboratory, for invaluable help in the work and in the revision of the manuscript.

The earlier view in regard to the origin of the sympathetic nerv ous system was that advanced by REMAK, to the effect that it arose in situ from the mesoblast. BALFOUR, after his researches on elasmobranch fishes ('78), brought forward a new view, namely, that the sym pathetic nervous system arises from the epiblast in connection with the spinal and with certain of the cranial nerves. He claimed that the sympathetic ganglia of the trunk region "are at first simply swellings on the main branches of the spinal nerves." Subsequently, these swellings are removed each from its respective nerve, retaining, however, fibrous connections with the nerve through a short branch, which forms a ramus communicans. They appear at first to be independent, becoming united later by commissures, and forming a continuous cord on either side.

1 Contribution from the Zoological Laboratory of Northwestern University, WILLIAM A. Locy, Director.

SCHENK and BIRDSELL published, in 1879, the results of their observations on certain mammalia, which, as BALFOUR says, "seem to indicate that the main parts of the sympathetic system arise in continuity with the posterior spinal ganglia; they also show that in the neck and other parts the sympathetic cords arise as a continuous ganglionic chain." ONODI ('86), working on elasmobranchs, agrees essentially with BALFOUR, and gives excellently clear figures intended to show that the cells which form the sympathetic cord arise as outgrowths from the spinal ganglia.

PATERSON, in 1891, revived the idea of the mesoblastic origin of the sympathetic nervous system. According to his researches on mouse, rat, and human embryos, the earliest traces of the sympathetic are seen as a cellular cord lying in the mesoblast between the aorta and the cardinal vein, in the anterior dorsal region. This cord is bilaterally symmetrical, and is composed of cells which he claims are differentiated mesoblastic cells. At the time of its appearance, the cord has no connection whatever with the spinal nerves nor ganglia, and constitutes the anlage of the sympathetic. The next step is the formation of the rami communicantes, which arise as fibrous outgrowths passing from the spinal nerves to the sympathetic cord. The ganglia appear next, and are formed at the points where the rami join the cord, resulting presumably from the growth of both sympathetic cells and nerve fibers. The collateral sympathetic is developed by the outgrowth from the sympathetic cord of cellular branches, which later give rise to the ganglia, nerves, and plexuses. In this category are placed the cervical and sacral portions of the sympathetic chain and also rather doubtfully, the grey rami communicantes. This view is repeated by PatERSON, in 1903, in Cunningham's Anatomy.

MARSHALL (93), on the other hand, agrees very closely with the theory advanced by BALFOUR. In frog and chick embryos, MARSHALL finds that the sympatetic nervous system arises "as a series of outgrowths from certain of the cranial and from all of the spinal nerves. These develop ganglionic swellings," which later become connected by fibrous commissures, thus forming the gangliated chain of the adult.

HIS, Jr. (97), tracing in the chick the history of an anlage similar to that described by PATERSON, finds, in very early stages, that the cells forming it come from the ganglia of the spinal nerves, thus confirming

the researches of ONODI ('86), on elasmobranchs. In the human embryo, His, Jr. finds that the development of the sympathetic begins (in a 10 mm. embryo) with the outgrowth of the white rami communicantes from the spinal nerves. A little later, the sympathetic cord appears and is joined by the rami. These findings contrast with those of PATERSON ('91), who observed that the structure first to appear is the sympathetic cord, the rami developing later.

HOFFMANN's observations on the sympathetic system of selachians ('99) agree, as far as essential features of development are concerned, with those of BALFOUR and ONODI. Like them, he shows that the cells forming the sympathetic anlage arise in connection with the spinal nerves, thus favoring the view that the sympathetic is epiblastic in origin. In urodeles, he finds ('02) the first trace of the sympathetic occurring as scattered cells connected by slender rami to the ventral branches of the spinal nerves. He does not express an opinion as to whether these cells are of epiblastic or mesoblastic origin. In 30 mm. salamanders, the sympathetic has come to be a continuous chain, in some places fibrous, in other places cellular in character, extending from the first spinal nerve back to the tail region and connected by rami to all of the spinal nerves.

Another question relates to the connection, during embryonic stages, between the sympathetic anlage and the adrenals. These two structures come into very intimate relation with each other during their development. In reptiles, there arises on each side of the vena cava soon after its formation a longitudinal cord of cells, which MINOT calls the "mesenchymal anlage" of the adrenals. On the dorsal side of this anlage and somewhat toward the median line, appear clusters of cells, which are derived from the sympathetic ganglia. They constitute the "sympathetic anlage" of the adrenals.

1

These two portions come in contact, and at first, in amniota at least, the sympathetic part grows more rapidly, and partially surrounds the mesenchymal portion; but soon the relations become reversed, and the mesenchymal portion gradually surrounds the sympathetic; what finally becomes of the latter is not known. BALFOUR (78) found in elasmobranchs, in the case of the posterior adrenals, that each of these bodies shows a small sympathetic ganglion attached to either end of it, the whole structure being attached to a spinal nerve by a ramus. This mass of cells gradually becomes divided into a ganglionic and a glandular portion; the latter acquiring a mesoblastic investment becomes adrenal, while the former develops into sympathetic tissue.

"Human Embryology." Pages 485 and 486.

MANN (99), working on selachians, confirms the findings of BALFOUR, in their essential features.

A brief summary of the literature embodies the following points: (1) The cells from which the sympathetic arises, probably come originally from the spinal ganglia, as shown particularly by BALFOUR ('78), SCHENK and BIRDSELL ('79), ONODI ('86), and HIS, Jr. ('97), PATERSON ('91) being the most recent investigator to hold to the mesoblastic theory. (2) In elasmobranchs, the sympathetic begins with the development of the ganglia, which arise as cellular outgrowths on the spinal nerves. These gradually are removed from the nerves, retaining, however, fibrous connections, which constitute the rami The commissures arise later, probably as outgrowths from the sympathetic ganglia. (3) In mammalia and in aves, the sympathetic appears first as a continuous longitudinal cord, which later is joined by rami communicantes, arising as outgrowths from the spinal nerves. At the points where the rami join the cord, ganglia develop, while the intervening portions of the cord remain as commissures. (4) The collateral sympathetic arises as outgrowths from the sympathetic cord. (5) A portion of the sympathetic anlage has, during its development, very intimate relation with the adrenals. (6) From an embryological as well as from an adult morphological and physiological stand-point, the sympathetic system is best considered as an integral part of the whole nervous system and not as a structure that is to any considerable extent distinct or separable from the rest of the nervous system.

cantes.

My own observations upon the development of the sympathetic nervous system have been confined mainly to the derivations of the ganglia, their commissures, and the rami communiThe observations were made upon toad and frog embryos, and were limited to the region posterior to the vagus ganglion. Graphic reconstructions were made from serial transverse paraffine sections, supplemented by actual dissections. For the sake of clearness, a general statement is given before proceeding to the description of particular stages of develop

ment:

(1) The sympathetic system between the vagus ganglion and the second spinal nerve, in the animals studied, appears to arise from cells scattered in the mesoblast of the region where the future sympathetic cord is to lie. A portion of these cells gradually becomes aggregated to form a cord (Fig's. 2, 7, and

8, Sy.) which is the beginning of the sympathetic as an anatomically distinct structure in this region. Scattered cells are to be seen among the fibers of the first and second spinal nerves, all the way up to the spinal ganglia. These cells become continuous below with the cells of the forming sympathetic cord. Also, there is a connection between the sympathetic cord in front of the second nerve and the group of cells which give rise to the sympathetic in the trunk region. These facts of observation favor the view that the cells which enter into the formation of the sympathetic cord anterior to the second spinal nerve migrate either (a) downward from the ganglia of the first and second spinal nerves or (b) forward from the structure which gives rise to the sympathetic of the trunk region, posterior to the second spinal nerve. However, the question of the origin of these cells requires further investigation.

(2) My preparations show that all of the sympathetic posterior to the second spinal nerve arises from an antecedent structure, which is bilaterally symmetrical, and lies closely applied to the dorsal and external side of the aorta, where the latter is double, and to the outer side of the median aorta, after the union of the two trunks. This antecedent structure consists of an irregular ridge of cells (Fig. 1, Ri.) extending back to the region between the ninth and tenth nerves (Fig. 7, Ri.), suffering interruption, however, in the region of the third. Throughout its entire extent, this ridge is continuous inferiorly with a mass of cells (Fig. 1, Ma.), which, between the second nerve and the anterior end of the kidney, lies between the aorta and the Wolffian duct (Fig's. 1, 3, 4, and 5, Ma.) and, in the region of the kidney, between this organ and the aorta (Fig. 6, Ma). It extends some distance anterior to the second nerve, where, however, its connection with the sympathetic is uncertain. This ridge (Fig. 8, Ri.) is continuous anteriorly with the sympathetic cord between the vagus ganglion and the second spinal nerve, and arises at the same time as this portion of the cord. The division of the forming sympathetic into a portion anterior to the second spinal nerve and one posterior to it is observed throughout the following descriptions.