Talk:Book - Manual of Human Embryology 14

From Embryology


The sympathetic system arises in common with the spinal ganglia from that portion of the ectoderm which forms the lateral border of the neural plate, and in common with the spinal ganglia it takes part in the formation of the neural crest. As the neural crest becomes detached and its segmenting parts invade the space between the myotomes and neural tube, certain ganglioncells separate themselves from its ventral border and independently migrate ventralward into the neighborhood of the aorta. It is these cells that form the connected chain of errant ganglia which we know as the sympathetic system. It is a true derivative of the rest of the nervous system. Originally the two were continuous ectoderm, and the establishment of the former as a distinct and separate system is solely due to its detachment and forward migration.

To witness the successive steps in the development of the sympathetic system it is necessary to commence with embryos that are still in the neural crest stage, 2-3 mm. long. At 7 mm. the cell migration is in active progress, and cellular rami communicantes are already present in some regions ; in the 9 mm. embryo the ganglionic cord and splanchnic nerve-plexus are definitely outlined; and finally, in the 16 mm. embryo the differentiation has advanced far enough so that it is possible to recognize the more outlying visceral ganglia and the ganglia of the head and their connecting branches. Thus, before the completion of the sixth week of embryonic life the essential features of the entire sympathetic apparatus can be clearly made out.

A representation of the derivation of the sympathetic cells is shown in Fig. 101, in which A, B, C, and D represent the successive stages and show schematically the increase in number and forward migration of cells and the subsequent formation of connecting fibre trunks. The sympathetic cells are shown in black in contrast to the other derivatives of the neural crest, — i.e., the sheath cells and the spinal ganglion-cells. The sheath cells are shown as plain white rings, while the spinal ganglion-cells are dotted.

Fig. 101. — Diagram representing the origin and migration of the sympathetic ganglion-cells and their relation to the other components of the neural crest. Sympathetic cells, black; spinal ganglion-cells, dotted circles; sheath cells, white rings. A and D are based on embryos Nos. 12 and 143 of the Mall collection, and B and C on the Buxton embryo, Gage collection.

The three varieties of cells mentioned can be traced back to the neural crest, as indicated in stage A. They are, however, not to be distinguished from each other histologically at this time; it is only for schematic purposes that they are represented in Vol. II.— 10 that way in the drawing. In the next drawing, B, can be seen the increase in size and ventral advance of the entire ganglion mass. The ventral advance is in part secondary to the increase in the number of cells and the consequent forward crowding in the direction of least resistance, and in part it is due to the intrinsic migratory energy of the individual cells. What appears as an ill-defined ragged ventral border, on closer examination can be seen to be made up of branching ganglion-cells reaching forward into the mesoderm in the form of a loose syncytium. In the drawing, for the sake of simplicity the processes are not shown. As seen in B, cells from the loose ventral border of the ganglion mass detach themselves and extend ventralward in advance of the ventral root fibres. The latter can be seen emerging from the neural tube and following along in the wake of the migrating ganglion-cells. Simultaneously with the forward growth of the ventral root fibres and the formation of a definite nerve-trunk, as shown in C, the sympathetic cells continue their migration medianward toward the aorta and thereby form a cellular connected strand which is the primitive ramus communicans. The difference between drawings B and C is that existing between the upper and lower parts of the spinal cord of the same embryo. B corresponds to the upper thoracic region in the 4.5 mm. embryo.

The completion of the segmental type is shown in D, where the sympathetic cells have completed their wandering, and by rapid increase in numbers form a compactly clumped ganglion mass which by fusing from segment to segment extends as a continuous longitudinal cord along the lateral border of the aorta. The cellular ramus communicans is in the meantime replaced by centrifugal fibres from the nerve-trunk which have followed along the migration path, the same fibres that form the white ramus in the adult. Somewhat later centripetal fibres sprout out from the sympathetic ganglia and either work their way backward along the path of the centrifugal fibres, or else form an independent bundle, the future gray ramus. The ramus communicans thus represents a portion of the path along which the sympathetic cells originally migrated. At first consisting of a chain of ganglioncells spun out by the wandering cells, it is later replaced by an ingrowth of fibres representing spinal axones on the one hand and sympathetic axones on the other ; the cells forming the temporary connecting bridge, having in the meantime completed their journey, form a compact ganglion mass near the aorta.

If we judge from the adult conditions we must conclude that there are some sympathetic cells which never wander out from the spinal ganglion mass. Some of these stationary cells are shown in the drawings C and D. Likewise some of the sheath cells do not leave, but remain in the ganglion mass, where they either

DEVELOPMENT OF THE NERVOUS SYSTEM. 147 form sheaths to the nerve-fibres or else form cell nests encapsulating the ganglion-cells proper. The wandering sheath cells, as seen in B and D, advance simultaneously with the sympathetic cells at the tip of and along with the nerve-fibres, and by the time a well-defined nerve-trunk makes its appearance sheath cells are found scattered along its whole course, as well as along the ramus communicans.

The development of the individual sympathetic ganglion-cell may be divided into three stages. The first, or indifferent stage, covers the period during which it is one of the cells forming the neural crest and spinal ganglion mass ; the second, or intermediate stage, corresponds to the period of migration; the third, or terminal stage, is from the time it reaches its permanent position to the attainment of its adult form.

During the first stage the three cell groups derived from the neural crest — i.e., the sympathetic ganglion-cells, the spinal ganglion-cells, and the sheath cells — cannot be distinguished from one another, and may be considered as indifferent ectoderm cells. Together they constitute a moderately compact mass lying between the neural tube and the dorsal border of the myotome. Their body-outlines are ill-defined and show more or less fusion. As compared with the adjacent mesodermal cells they possess more body protoplasm and are not branched. The nuclei are oval or rounded and are marked by deeply staining nucleoli.

During the second or wandering stage the sympathetic cells, as is common with all wandering cells, are characterized by the development of slender protoplasmic processes. The sheath cells also develop similar processes about the same time, and the two cannot be easily distinguished from each other. The nuclei of the latter, however, are somewhat more elongated and take the stain less intensely. The spinal ganglion-cells may be readily identified by the well-defined protoplasmic body which the more advanced ones have in the meantime developed. It is proposed by Kohn (1905) that the sheath cells of this period and the sympathetic cells, because of their similarity and their prevailing presence along the developing nerve, be grouped together under the term neurocytes. A syncytial strand of this type of sympathetic cells forms the initial ramus communicans. which can be seen making its way through the mesoderm toward the aorta, entirely devoid of fibres. See accompanying Fig. 102, which shows a similar picture in the rabbit.

With the beginning of the third stage the sympathetic cells undergo their terminal differentiation. They rapidly proliferate and clump themselves into ganglia; while the individual cells develop condensed and sharply outlined protoplasmic bodies and their processes become fibrillar and extend out to take part in the formation of the various communicating trunks. In passing through these three stages the sympathetic cells do not all develop with equal rapidity, and there is consequently an overlapping of the successive periods; for example, the cells belonging to the ganglionated cord are well along toward the completion of the third stage at a time when the visceral ganglia are still in the second stage, and likewise some parts of the ganglionated cord develop

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Fig. 102. — From a cross section through a rabbit embryo, showing chain of sympathetic cells forming the primitive ramus communicans {re), which leads from the fibrous spinal nerve (n) medianward toward the aortic region. Enlarged 300 : 1. nz. neurocytes ; bk, blood-cells. (After Kohn, 1907.) more rapidly than others, the thoracic region is always in advance of the lower lumbar and sacral and the cranial ganglia.

The earlier writers (Remak, 1847) were of the opinion that the sympathetic system was of mesodermal origin, until Balfour (1877) showed that in selachians the sympathetic ganglia develop as buds or outgrowths from the trunks of the spinal nerves, and hence are ectodermal. Some observers (Pater son, 1890) still adhered long after to the mesodermal origin, yet Balfour's observations were thoroughly confirmed and the ectodermal origin of the sympathetic was generally regarded as thereby established. Later investigators (Schenk and Birdsall, 1878, Onodi, 1886), who worked

DEVELOPMENT OF THE NERVOUS SYSTEM. 149 on higher forms, including human, modified Balfour's view by describing the sympathetic ganglia as detached parts of the spinal ganglia which are separated off and linked together into a longitudinal chain. It was not until His, jun. (1891), introduced the principle of the wandering of individual sympathetic cells that we approached our present conception. It was surmised by His (1890) and immediately supported by His, jun. (1891), that the development of the sympathetic system is dependent on the active ventral migration of germinating sympathetic cells, which cells, however, do not migrate until a preliminary nerve-fibre framework is laid out in the form of rami communicantes and connecting longitudinal commissures. Along these fibre paths the sympathetic cells wander forward to form ganglia.

The only essential difference between the description of His, jun., and that as given above in the present article, consists in the time of cell migration. The writer is in accord with the recent work of Kohn (1907) in believing that the migration occurs earlier than described by His, and that the cells wander through mesoderm rather than along compact nerve-fibre paths. The same picture is presented in human material that Kohn describes in the rabbit : migrating cells can be recognized in advance of the loose strands of the tip of the growing nerve, and extending through the mesoderm as a bridge of cells toward the aorta; by the time a well-defined nerve-trunk is established the sympathetic cells have already completed that part of their migration, and the cells then found on the nerve-trunk are sheath cells only. A divergent view has been recently published by Cajal (1908), according to which the sympathetic cells in the chick are true motor cells and are derived from the spinal cord. During their germinative stage they migrate out from the cord at the same place at which later the ventral roots emerge.

The cranial sympathetic system departs from the uniform segmental type found in the trunk. It, however, adheres in three ways to the general type: first, the ganglion-cells are apparently derived from a cerebrospinal ganglion mass; secondly, they migrate ventralward and eventually assume a position outside of the bony canal, and thirdly, the ganglia give off fibres which form a communicating trunk along the internal carotid artery, this trunk serving to unite the cranial sympathetic ganglia with each other, analogous to the longitudinal system of communications of the ganglionated cord, with which it is continuous.

The early history of the cranial sympathetic ganglia is less definitely known than that of the trunk system, due to the relatively smaller size, lesser number, and lack of symmetry of the former ganglia, as well as the complexity of the surrounding struc tures. From the evidence at hand it seems probable that all the


cranial sympathetic ganglia — gg. ciliare, sphenopalatinum, oticum, and submaxillare — are originally derived from the semilunar ganglion mass.

The ciliary ganglion presents certain modifications. In the chick it consists (Carpenter, 1906) of two portions, a smaller dorsal sympathetic portion derived from the semilunar ganglion, and a larger ventral portion containing large bipolar cells (supposedly sensory), derived from the neural tube by migration along the oculomotor nerve. In the same way in the torpedo it is known that cells wander out from the medullary tube and migrate ventralward in company with the growing oculomotor fibres, and eventually fuse with the cells derived from the trigeminal ganglion, together forming a composite ganglion (Froriep, 1902). If there are any oculomotor ganglion-cells in the human embryo, such as are found in the chick and torpedo, they do not apparently pass through a migrating stage, and never leave the neural tube. Consequently the ciliary ganglion here consists exclusively of migrant cells from the semilunar ganglion. We may assume that they behave like the sympathetic cells of the trunk and pass through their wandering stage very early. Their detachment from the parent ganglion mass and forward migration must occur just in advance of the developing nerve-trunks, and it is not until they reach their permanent position that they undergo active proliferation and form a compact cell group.

Both the sphenopalatine and submaxillary ganglia are probably derived entirely from the semilunar ganglion, but it must be borne in mind that they are connected with the geniculate ganglion of the facial, and there is the possibility that the former contains contributing cells which have migrated along the path of the great superficial petrosal nerve and the latter cells which have migrated along the path of the chorda tympani. In the same way the otic ganglion, though developed intimately with the semilunar ganglion, may in part consist of cells derived from the glossopharyngeal nerve through its tympanic branch. However, both their comparative and embryological histories indicate that the facial, glossopharyngeal, and vagus nerves constitute a definite group, one of the characteristics of which is that they retain within their root or trunk ganglia or within the brain tube itself whatever sympathetic ganglion-cells they possess, and consequently there are in connection with them no rami communicantes and no derivative ganglia.

The origin of the four cranial ganglia may be represented as in the adjoining scheme, Fig. 104. The arrows indicate the paths of primary migration, and the dotted lines paths of subsequent intercommunication, by which all the cranial ganglia establish connection with the carotid plexus and so become directly continuous



with the gangliated cord of the trunk. This figure should be compared with Fig. 103, which represents a profile reconstruction of an embryo 16 mm. long. For the purpose of contrast the sympa

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Q nodos.

Tr'uncus sympathicus Fio. 103. — Profile reconstruction of the sympathetic nervou9 system in a 16 mm., nearly six weeks, embryo (Huber collection, VI), enlarged 10 : 1. In order to expose the cceliac plexus and suprarenal gland the stomach is represented as raised forward and to the right.

thetic system is shown in black. The cranial sympathetic ganglia at this time are connected with the semilunar ganglion by longer or shorter branches which are analogous to rami communicantes.


The ganglion ciliare lies closely against the oculomotor nerve, from which it receives some fibres. A true ramus communicans, identical with the radix longa of the adult, connects it with the ophthalmic division of the trigeminal nerve. The sphenopalatine ganglion is connected with the parent ganglion by two or more rami communicantes, the nn. sphenopalatine These are in part sensory fibres, which pass' directly through the ganglion without interruption, connecting the periphery with the semilunar ganglion. It is fibres % of this sort that form the major part of the peripheral branches of the ganglion. In case of the otic ganglion there is a less distinct ramus communicans, owing to the fact that the ganglion lies closely against the nerve-trunk and thus there results in the adult a short plexus uniting the two. The submaxillary ganglion presents an even more close union between the ganglion and the nerve-trunk, and the latter in 16 mm. embryos can be seen making its way directly through the substance of the ganglion mass. So here, as in the case of the otic ganglion, there results a plexus of communication between ganglion and nerve-trunk. In speaking of this as the ganglion submaxillare it is done in the sense of including both the submaxillary and sublingual ganglia. As has been shown by both Langley and Huber (Huber, 1896), that which is ordinarily referred to as the submaxillary ganglion is in reality sublingual, while the submaxillary ganglion proper consists of multiple ganglia situated in the substance of the gland along the course of its ducts.

It was shown in Figs. 101 and 104 how the sympathetic cells in the spinal region migrate forward and form ganglia, and it has been also mentioned that these ganglia fuse from segment to segment and thereby form a continuous longitudinal cord of ganglioncells, the so-called ganglionated cord. This structure is at first purely cellular. Later, fibres make their appearance among the cells; in the 16 mm. embryo, Fig. 103, they are already abundant, particularly in the cervical and thoracic regions. The fibre growth continues in such a manner as to break the continuity of the cellular cord, and produces a longitudinal series of ganglionic masses connected by intervening fibrous bridges, the ganglionic chain as seen in the adult. For the greater part these ganglia are segmental, but in the cervical and upper thoracic region the cells remain massed in larger clumps, and there result ganglia corresponding to from two to five segments.

The prevertebral and visceral sympathetic ganglia are considered by most writers as derivatives of the neural crest in common with the rest of the sympathetic system. They differ only in that their migration extends further than that of the latter: instead of stopping at the side of the aorta, they migrate ventralward through the loose mesoderm into the region of the preverte



bral plexuses, and some of them still further forward to become incorporated in the walls of the viscera to form the submucous plexus. These paths of migration are diagrammatically shown in Fig. 104. These ganglia reach their eventual position relatively early, so the distance covered in their migration is therefore not so great. Cajal (1908) describes in the chick of 52 hours visceral

Q ciliare

G. sphenopal Q. submax

Pix coeiiacus Pix submucosus

Pix hypoqastr

Fig. 104. — Diagram showing the migration paths of the sympathetic cells. Dotted lines indicate secondary subsequent communications which link the ganglia together and form a longitudinal chain continuous throughout head and trunk. Secondary and tertiary migrations result in the formation of prevertebral and visceral plexuses.

sympathetic cells which have completed their migration. In human embryos 16 mm. long the cardiac ganglia are to be recognized. The main features of the cardiac plexus are completed by the time the embryo reaches 19 mm. neck-rump length, as shown in Fig. 105. The cceliac and hypogastric plexuses together with the splanchnic nerves present the picture seen in Fig. 103, and differ from the adult only in the incomplete differentiation of the cells. Continuous with the cceliac plexus is a group of sympathetic

154 cells which extend through its median surface directly into the substance of the suprarenal gland, and constitute its nerve supply. A portion of these cells, instead of becoming typical ganglioncells, undergo special development, the details of which are not yet satisfactorily understood. On account of the affinity of these

N. vagus


Bulbar plexus


Truncus sympathicus

Connecting plexus

Atrial plexus

Fig. 105. — Cardiac rlexua in human embryos between 10 and 19 mm. long. (After Kollmann, 1907, and iHis, jun.. 1891.) special cells for the chrome salts, they are designated as chromaffin cells. They are found also in other portions of the sympathetic system, such as in the ganglia of the ganglionated cord and of the abdominal plexuses; to some extent they also form independent bodies, the chromaffin bodies of Zuckerkandl, to which group the carotid glands belong. These structures will be described in detail in the following chapter.


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