Paper - Problems concerning the origin and development of the neural crest and cranial ganglia in the vertebrates (1928)

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Stone LS. Problems concerning the origin and development of the neural crest and cranial ganglia in the vertebrates. (1928) Yale J Biol. Med. 1(1): 7–14. PMC2606212

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This historic 1928 paper by Stone describes an early understanding of neural crest and cranial ganglia (cranial nerve) development in vertebrates.

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1879 Olfactory Organ | 1905 Cranial and Spinal Nerves | 1908 10 mm Peripheral | 1910 Mammal Sympathetic | 1920 Human Sympathetic | 1928 Cranial ganglia | 1939 10 Somite Embryo | 1942 Origin | 1957 Adrenal

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Problems Concerning the Origin and Development of the Neural Crest and Cranial Ganglia in the Vertebrates

L. S. Stone

From the Department of Anatomy, Yale University School of Medicine.

In the present period of the history of the science of embryology, much attention is focused upon its recent advancement due chiefly to the influence of the introduction of experimental methods in attacking its problems. For the reader who cares to inform himself of some of the phases of this fascinating and youthful science the recently published volume Experimental Embryology, by Thomas Hunt Morgan, will be of great interest.

It may be said that of the various developmental systems of the embryo the nervous system has perhaps presented some of the most interesting problems which have lent themselves to an experimental analysis. It is to some of the experiments upon this system that attention is here called.

For the past few years interest has been centered about problems dealing with the origin and development of cranial ganglia in vertebrate embryos. Some of the problems which this subject presents, and the results obtained by the methods of approach to these studies which laid the background for our present knowledge of this subject will illustrate in a way the relationship of the purely descriptive to the experimental embryologist and will show how far each, with the limitations of the methods that he applies, is able to proceed toward the solution of the problem in hand.

Without giving an historical background of the complex problems involved it is sufficient to say that concerning the origin and development of cranial ganglia and their nerves all classes of vertebrates from fishes to man have been studied by the purely descriptive embryologist. In order to make such a study in any animal the descriptive embryologist must first obtain embryos closely staged in order of sequence from early to late periods of development. From these embryos his chief source of material for study consists of preparations of serial miscroscopic sections stained in the proper manner to give cellular detail. Of course in such investigations progress goes hand in hand with the development of the technic that makes it possible to obtain the most desirable sections for microscopic studies. The descriptive embryologist usually begins his observations of the particular ganglion or ganglia, as the case may be, at the stage of development where he can identify the exact position and appearance of the cells in question. From that point he may study progressively back through each succeeding younger stage until the identity of the cells is no longer distinguishable, or until, if he is fortunate, he fixes their point of origin. In so doing he discovers the critical changes in the development of the ganglion and its relation to the developing structures surrounding it. On the other hand, he may find as he progresses through the earlier stages of development that cells surrounding the ganglion may become so intimately related with that structure that his conclusions formulated from such an obscure picture are open to question.

However, a similar cranial ganglion may, in the embryos of another closely related vertebrate, present a less complicated picture and hence may give assistance in interpreting the more obscure one. The descriptive embryologist often resorts to such assistance in his studies. But such conclusions may still remain open to question due to the fact that cells microscopically quite similar to the ganglion-forming cells are always migrating through or around the region of the ganglion at certain early stages, constantly presenting a very difficult picture to understand. So the descriptive embryologist with the limitations of his methods must collaborate with the experimentalist, but even the latter must turn to purely descriptive methods from time to time.

Concerning the development of cranial ganglia the fishes and amphibians have received the greatest attention and of these we possess more knowledge about the conditions in the amphibians than in any other single class of vertebrates. It has long been known that at about the time the neural folds fuse to form a neural tube cells proliferate from the dorsal ridge or crest of the early forming tube and move ventrally over its sides. These cells of ectodermal origin are called the neural crest cells. As early as 1878 attention became focused upon these cells and soon various studies were begun to determine their ultimate fate. Observations tended to show that the neural crest cells were not only concerned with the formation of certain cranial nerve components but that some of these cells wandered away from the nervous system and became intimately related with, and eventually lost among, cells of another germ layer, the mesoderm. Soon intimations were made that these migrating neural crest cells formed tissues which were formerly believed to be derived exclusively from other cells, viz., mesodermal cells. This interpretation was, and still is by some, vigorously attacked in defense of the integrity of the germ layer theory of development. This theory has had a wide-spread influence in the field of embryology for it concedes to each of the primary germ layers, ectoderm, mesoderm, and endoderm, the origin of definite organs and tissues. Therefore, any observations which did not fall in with this point of view were looked upon with scorn.

In the early nineties it was shown that in the head region localized areas in the ectoderm, now called placodes, shed off cells into the region where neural crest cells are also to be found. At various periods extending down to the present time a number of investigators have corroborated these observations, thus establishing a fact which made the picture still more difficult to interpret. The apparent intermingling of cells from placodes of the lateral ectoderm with those of the neural crest gave rise to variously opposed points of view and thus the question of the origin of cranial nerves and the fate of the crest cells became more complex instead of becoming more simple.

Amphibian embryos provided very favorable material for such studies and in these forms many observations have been recorded. Microscopic characteristics of neural crest and placodal cells, such as the size of the cells, the size and amount of yolk-granules present and the pigmentation, gave some measure by which they could be followed and differentiated from surrounding cells during certain critical periods in development. These characteristics were emphasized largely by F. L. Landacre, particularly in his work on amphibians and have been confirmed by the writer.

Such were the complex pictures then which presented themselves and left unsettled for many years the question of the origin and development of the cranial ganglia. With the valuable background already furnished by the purely descriptive embryologists, attention was directed to an experimental analysis as an approach to the solution of these problems. Since the amphibians appeared to be best adapted to this procedure and because of their unique position in the vertebrate scale an investigation of this nature was undertaken upon embryos in this class of vertebrates and the first results were published by the writer in 1921. The well-known method of embryonic surgery developed by Harrison was adopted in obtaining the experimental results. Simply stated, this procedure consists of the manipulation of finely sharpened iridectomy scissors and suitable needles in a field under the compound dissecting microscope. The site of operation is highly illuminated by means of heat-filtered light rays centered upon an embryo placed in a black wax dish containing a very dilute salt solution. Asepsis is not required for work on amphibian embryos. By means of the operating instruments the desired area in the embryo is excised, after which healing is allowed to take place, a process that usually requires less than an hour for completion, if the wound is not large. If, however, it is desired to place into such a wound a graft from another embryo, then a donor embryo lying near the recipient is prepared as in the case of any excision. The transfer is carefully made with the assistance of the operating instruments and the transplant is oriented as desired, care being taken that the denuded area is of sufficient size to fit the graft. The recipient embryo rests in a slight depression in the wax dish and is further held in place by tiny silver wires banked about it. The graft is held in place while healing by means of a small glass rod gently resting upon it for a period of usually less than half an hour. The embryo operated upon is then transferred by means of a glass pipette to a dish containing fresh cool dilute salt solution and is kept for a few days in a chamber around which cool tap-water is kept running. The temporary cool environment seems to reduce the percentage of deaths, a possible subsequent event which in many cases is largely dependent upon the type of operation involved. Eventually the embryos are placed in fresh cool tap-water and brought to ordinary room temperature where they are allowed to develop to the stages desired for microscopic studies.

Upon the information already available the purely descriptive methods have also been applied in locating the position of various placodes or ectodermal thickenings in the head region of early embryos and in studying their development through the early critical periods. The neural crest was also followed through the early stages of development so far as this method of approach could be carried and these observations were checked against the experimental results.

It is obvious that if a certain group of cells, whether of a placode or of neural crest, are excised at a very early stage in development without otherwise disturbing the normal growth of the embryo we can discover later what structures are missing and therefore, we are in a position to verify or disprove many of the conclusions reached from purely descriptive studies. By implanting the embryonic transplant to another embryo, in any position we choose, we can observe later in the region of the graft whether or not there is developed the structure missing from the donor. We.can also go a step further. From our purely descriptive studies we can, for example, locate the position of the earliest microscopic appearance of what we believe to be the future ganglion-forming material. With that position in mind we can excise areas in much younger embryos where such microscopic evidence is lacking and into that wound we can graft a piece of indifferent ectoderm from the belly surface of another embryo which has been previously stained by a vital dye, such as Nile blue sulphate. This will then give us a blue area which can be followed for many days after operation. If that area lies in a position at a later stage of development where we know a certain structure should lie we possess a method of gradually working back to the earliest stage in development, when the particular structure in question is laid down in the embryo, by knowing how early before any microscopic evidence is revealed we can eliminate the structure from the host. These have been the methods employed in various studies of the origin and development of the cranial ganglia and the so-called neural crest.

Without entering into the details of many experiments which these studies have involved let us consider briefly the main results which they have shown. The experiments have proved beyond all reasonable doubt that in both salamanders and frogs the anterior portions of the trabeculae in the skull, the cartilagenous lower jaw and a large quadrate cartilage connected with it and the ear capsule, and the cartilagenous skeleton for the attachment of the gills of the larvae—a considerable amount of cartilagenous tissue—are all derived from those divisions of the cranial neural crest which migrate ventrally in the early embryo in great masses away from the nervous system. The experiments have also shown that some of the crest cells give rise to loose connective tissue about the mouth region and in the core of the gills of the larval stage. We have proof then that the neural crest which is ectodermal in origin, having come from the ectodermal neural tube, gives rise to structures such as cartilage and loose connective tissue, which, according to the older concept of the germ layer theory, could be derived only from mesoderm. It should perhaps also be mentioned here that Harrison showed a number of years ago that the sheath cells about the nerve fibers are also derived from neural crest, another non-nervous contribution of these cells.

To add further proof that the migrating neural crest cells form cartilaginous tissue, these cells were transplanted to the side of the body and to the inside of the brain cavity of very early embryos. In these positions there developed from the grafts cartilaginous bars corresponding in size to the amount of neural crest transplanted. When only the mesoderm, over which the neural crest normally migrates, was transplanted to new positions on the side of the body, muscle and blood vessels but no cartilaginous tissue developed in the site of the graft.

The cartilaginous skeleton of the head in vertebrates has been studied extensively in many forms. Its various parts in each class have been homologized from a phylogenetic point of view giving us our present conception of the comparative morphology of the head skeleton. Therefore, our knowledge of the origin and development of the skeleton of the head in amphibians, now placed upon a firm experimental basis, will give an interesting and valuable background upon which to base a reinvestigation of the development of the head skeleton in other vertebrates, including man, to discover whether or not the neural crest in these forms also plays the same réle as it does in amphibians.

Some of the descriptive embryologists adopted the point of view that the neural crest formed only ganglia. We have shown that this view is not correct. Other investigators were, and still are, divided in their opinions as to how much placodes and neural crest contribute to the formation of the cranial ganglia. Without entering into a detailed discussion of each cranial ganglion with its various components the chief results which an experimental analysis has revealed may be summarized somewhat as follows.

When only the cranial neural crest was excised it was found that with the exception of a deficiency in the general visceral system —a relatively small part of the cranial ganglia—all the components of the cranial ganglia were present. On the other hand, when all the placodes were removed, all the components of the ganglia were absent with the exception of the general visceral system. Thus it is shown that the placodes or ectodermal thickenings contribute much to the formation of the cranial ganglia. It was found in further experiments that when these placodes were transplanted to new positions on the body of the embryo they gave rise to ganglia in their new positions even though the location of the grafts was far from the central nervous system. It was further found that double ganglia could be produced if an extra placode was grafted into a position near a similar normal one of the host. And furthermore, it was found that certain placodes giving rise to ganglia of similar function could be interchanged, in each case forming a ganglion in place of and assuming the function of the one for which it was exchanged.

Thus we have, in a very limited field of research, briefly touched upon the relationship of the purely descriptive and experimental embryologist as to the methods of approach which each has taken in searching for the truth. The former points out the difficult barriers in the path of his progress. His judgment ofter later proves to be amazingly accurate in spite of the limitations of the methods at his disposal, even though at first his conclusions are not accepted as final proof. The experimentalist can take over the problems by applying a different method of attack and can often, but not always, find the way to a final solution which the descriptive embryologist is not able to obtain. He can take a step forward by a new pathway and can often discover new fields for research unrecognized by his companion in research. As codperative programs of investigations become more fully developed we shall have a more happy balance between the descriptive and experimental embryologist. We shall then, perhaps, not so often lose sight of the importance of the great contributions which the purely descriptive embryologist is constantly making, even though the experimental method may often yield more spectacular results.

Cite this page: Hill, M.A. (2024, May 25) Embryology Paper - Problems concerning the origin and development of the neural crest and cranial ganglia in the vertebrates (1928). Retrieved from

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