Paper - The development of the hypoglossal ganglia of pig embryos

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Prentiss CW. The development of the hypoglossal ganglia of pig embryos. (1910) J. Comp. Neural. and Psychol. 20(4): 266-282.

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Mark Hill.jpg This 1910 paper by Prentiss describes hypoglossal ganglia (CN XII Hypoglossal) development in the pig embryo.



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The Development of the Hypoglossal Ganglia of Pig Embryos

C. W. Prentiss

Northwestern University Medical School

Eight Figures

Introduction

The use of dissected pig embryos for classwork in embryology suggested itself to the Writer some years ago. Upon trial it was found that very instructive preparations could be made and with much greater ease than might be expected. It is difficult for students to grasp the relations of developing organs as seen in sections and as dissected embryo showing the primitive organs in position is very helpful in remedying this evil. It is the intention of the author to present, in a future paper, the results of his work along these lines, with directions for dissection and figures of the more instructive preparations. The form and relations of the various organs may be seen as accurately as in reconstructions made from serial sections by experts. There is this disadvantage in dissection, that some of the finer details of structure may be lost. For research it commends itself as a check to errors Which may occur in making reconstructions; for it enables one in a short time to study a considerable number of embryos.


The nervous system lends itself most easily to dissection. The mesenchyma crumbles away from the more tenuous nervous tissue of suitably prepared embryos, making it possible to lay bare the entire nervous system of pigs varying in length from 6 to 20 mm. The smaller embryos are more easily dissected, as no cartilage or bone is encountered.


My dissections brought out some points in connection with the cerebral nerves which have not hitherto been cleared up, and my purpose in the present paper is to describe the rudimentary gan glia which occur between the first cervical nerve and the vagu S, ganglia which I shall refer to as the hypoglossal ganglia because of their undoubted connection with this nerve. My descriptions will necessarily deal with the development of the last four cranial nerves, the glosso-pharyngeal, the vagus, the spinal accessory, and the hypoglossal.


Literature

The occurrence of hypoglossal ganglia was first described by Froriep (’82) in the sheep and the ox. He traced the development of a single ganglion, anterior to the first cervical, which it resembled in form, though smaller in size. The single distal root of this ganglion joined the most caudad root of the hypoglossal nerve. Anterior to this hypoglossal ganglion the neural crest was undifferentiated. Froriep and Beck (’95) found a precerVical ganglion present in the adult throughout those groups of mammals in which the first cervical ganglion was well developed.


Martin (’91), investigating cat embryos, found five ganglionic masses posterior to the jugular ganglion, and five roots of origin for the hypoglossal nerve. He concludes, therefore, that these ganglia are the dorsal ganglia of the hypoglossal, though he gives no figures in support of his view.


Lewis (’03) in his excellent paper on the anatomy of a 12 mm. pig found extending caudad from the jugular ganglion “ a beaded commissure ending in a small knob. In the track of the commissure, but separated from it, is an irregular ganglionic mass. After another interval there appears a small fragment, then follows the first cervical ganglion.” In one case he found a small fiber bundle connecting the irregular ganglionic mass (Froriep’s ganglion) with the hypoglossal nerve, but considers its “relation with the commissure ” as “far more striking than its resemblance with a spinal ganglion.” He finds the ganglion “connected with the commissure in pigs of 17 mm.” In a dissected pig of the same length “the hypoglossal ganglion appeared as a detached part of the ganglionic chain running forward to the vagus. This commissure could not be subdivided into definite ganglia; it was characterized by irregular swellings and spurs.”


Streeter (’04) in tracing the development of the peripheral nerves in human embryos finds a ganglionic crest extending from the first cervical to the superior ganglion of the glossopharyngeal and partly ensheathing the fibers of the spinal accessory nerve. In embryos 10 to 13 mm. long the neural crest becomes differentiated into four or five rather diffuse cell masses. Froriep’s ganglion resembles the others, being irregular in form and without roots. The hypoglossal nerve originates as four or five parallel roots. There is no correspondence between these and the rudimentary ganglia, nor are the ganglia segmentally arranged. He considers the three or four anterior cell masses as cerebral ganglia and “not to be confused with the precervical ganglion of Froriep.”

Materials and Methods

The number and length of the embryos dissected are given in the following table:


Length Of Example

Number Dissected


Stage Length


I 5- 7 mm. 6mm. 5 II 8-10 mm. 8.5-9 mm. 4 III 12-14 mm. 13—13.5 mm. 10 IV 17-20 mm. 17-18 mm. 10 V 28-30 mm. 28 mm. 4 41-50 mm.

All drawings were made with the aid of an Abbe camera lucida and a Zeiss a* objective. The embryos were fixed in Zenker’s fluid and the dissections were first stained, cleared in creosote and drawn as transparent objects. It was thus possible to locate microscopic cell masses and trace the course of very small fiber bundles. The dissection was then transferred to alcohol and examined as an opaque object by reflected light to obtain the contour of the different structures. By making several dissections of the same stage I believe that the finer structures were more accurately and completely reproduced than could be done by serial reconstructions.

Description of Dissections

Stage 1. 6 mm. In this embryo (fig. 1) the ganglia were connected from the glossopharyngeal (IX) back to the caudal region by continuous bands or loops of cells, undifferentiated portions of the neural crest. The ventral roots of the spinal nerves (0; C2) are large, but the dorsal ganglia show little differentiation into fibers, though short distal and proximal roots are present. The hypoglossal originates as five or six parallel roots, resembling those of the spinal series but uniting, in the later embryos of this stage, to form a common trunk (XII). The spinal accessory (XI), as an arched bundle of fibers, could be traced from the fourth cervical ganglion cephalad to the vagus. Dorsal to the accessory and partly ensheathing it is a flattened band of cells, the neural crest (crist. nemx), extending forward to the jugular ganglion of the vagus (gang. jugul.). Opposite the posterior root of the hypoglossal a marked ventral loop and thickening in the crest (gang. Froriep) shows the position of Froriep’s ganglion. Anteriorly the crest of cells is broader and a few short proximal rootlets are present. A depression separates it more or less completely from the cells of the jugular ganglion which is flattened and diffuse with 8-10 short proximal roots. The glossopharyngeal is short and its superior ganglion is joined to the jugular ganglion by a small cord of cells.



FIG. 1. Dissection of a. 6 mm. pig showing in the hypoglossal region the undifferentiated neural crest. See explanation of figures on page 282.



The remarkable features at this stage are then: the early development of the spinal roots; the resemblance of the hypoglossal to a series of ventral spinal roots; the existence of a nearly undifferentiated neural crest between the jugular and the first cervical ganglion.


Stage 2. 8.5-9 mm. In embryos of this stage (figs. 2 and 3), the roots of the spinal nerves are longer and more fibers. are developed. The first cervical ganglion is distinctly double in fig. 2. It is still connected with the second cervical ganglion by a loop of cells. The neural crest between the first cervical and the jugular ganglia shows the most marked change. The slight enlargement opposite the posterior root of the hypoglossal which we saw in the first stage has now grown to be a spindle-shaped mass of cells (gang. Froriep) with two proximal roots and a distal bundle of fibers which extends to the root of the hypoglossal. This ganglion (Froriep’s) is still connected with cellular loops (nod.) of the neural crest, but in this respect it does not differ from the cervical and sacral ganglia of this stage. It strongly resembles one of the two cell masses composing the first cervical ganglion. Anterior to it is a smaller mass of cells (gang. hypogl.) from which a proximal root is developing. This is the “terminal knob”-of the “commissure” figured by Lewis in the 12 mm. pig (1903, pl. I). Anteriorly the crest shows five diffuse irregular cell masses which become gradually larger toward the jugular ganglion with indications of proximal roots. The jugular ganglion is of more definite form and is pointed ventrally. Dorsal mgelencephulon to the ganglion nodosum of the vagus (gang. nodos.) a small bundle of fibers is given off to form the peripheral portion of the spinal accessory (XI ’ ).


FIG. 2. Dissection of an 8.5 mm. pig showing Froriep’s ganglion with a distal root to the hypoglossal nerve, and a double (cervical ganglion.


FIG. 3. Dissection of a. 9 mm. pig showing an early stage in the differentiation of the neural crest to form the hypoglossal ganglia.



Two embryos of 8.5 mm. showed the structure of fig. 2. In two others of 9 mm. no distal root has developed from Froriep’s ganglion (fig. 3). The first cervical is not distinctly double and shows no connection with the second cervical ganglion. The proximal roots are longer, however, and the neural crest near the jugular ganglion is better differentiated. Two flat distal strands of mixed cells and fibers pass down parallel to the spinal accessory fibers and enter the vagus.



FIG. 4. Dissection of a 13 mm. pig to show a seiies of hypoglossal ganglia and two double cervical ganglia.


This stage brings out three important points: (1) the first cervical ganglion frequently originates as a double structure; (2) Froriep’s ganglion sends fibers to the hypoglossal at an earlier stage than has been described by other investigators; (3) its resemblance to one of the divisions of the first cervical ganglion is marked.


FIG. 5. Dissection of a 13 mm. pig showing a series of eight hypoglossal ganglia and the persistence of the neural crest from the superior ganglion to the first cervical.


Stage 3. 13 mm. This embryo, of about the same age as that studied by Lewis, is characterized by a further elongation of the distal and proximal roots and by a greater differentiation of the neural crest anterior to the first cervical nerve. Five of the ten embryos dissected belonged to the types shown in fig. 4 and fig. 5. Here we see a cord of cells passing cephalad from the first cervical ganglion. In fig. 5 it joins Froriep’s ganglion. In fig. 4 it passes under its proximal roots. Froriep’s ganglion possesses now one, now two proximal roots, with a distal bundle of fibers entering the posterior root of the hypoglossal nerve, and it is united to a more irregular ganglionic mass by a strand of cells which Varies in size in different embryos. This second ganglion also shows one or two proximal roots, and a distal root is in evidence. A third cell mass more eephalad shows a proximal root, is pointed at its distal end and projects ventrad to the spinal accessory. Anterior to these three occurs a series of five cell masses, more diffuse, more closely united and elongate in the antero-posterior line. A small strand of cells unites the more eephalad of these to the jugular ganglion, and this in turn is connected with the superior ganglion of the glossopharyngeal. Each of these cell masses possesses from two to four proximal roots, and two pairs of the adjacent roots are joined by cellular loops. Distal roots either join the spinal accessory or form part of flattened bundles which pass to the trunk of the vagus.


In three of these five embryos the first cervical ganglion was distinctly double as in figs. 4 and 5. In the other two it gave evidence of a double origin. An interesting point was the difference in structure exhibited on the right and left sides of the same embryo. For example, in two other cases Froriep’s ganglion was well developed with a distal hypoglossal root on the right side, small and without hypoglossal root on the left side. In two cases no hypoglossal root was found on either side, a condition similar to that figured by Lewis, who, however, found a small distal fiber bundle in a second embryo.


To sum up: The 13 mm. embryo shows (1) the neural crest anterior to the first cervical ganglion differentiated into about eight ganglionic masses; (2) the two posterior of these send roots to the hypoglossal in the majority of cases, and the condition figured by Lewis is apparently the exception rather than the rule; (3) a persistence of cellular cords still unites the various links in this chain of ganglia with each other and with the first cervical and jugular ganglia; (4) the first cervical ganglion is often double in structure, and all the spinal ganglia are elon.gate and unlike the rounded nodules figured by Lewis; (5) in the ganglionic chain it is not possible to distinguish an anterior cranial series belonging to the vagus complex, and a pre-cervical group of spinal ganglia as maintained by Streeter C04); (6) the connection between the chain of ganglia and the Vagus is not as marked in most cases as Lewis figures, and when well developed represents a persistence of the ganglionic crest — a persistence common also to the spinal ganglia; (7) the spinal accessory root could be traced back to the sixth cervical ganglion.



FIG. 6. Dissection of a 17 mm. pig showing three distal roots passing from the hypoglossal ganglia to the ventral roots of the hypoglossal nerve and a fourth incomplete root.



Stage 4. 17-18 mm. Further elongation of the nerve roots is accompanied by a differentiation of the hypoglossal ganglia greater than at any other stage (figs. 6 and 7). The ganglia are relatively smaller but a continuous cord of cells may still be traced from the first cervical to the jugular ganglion. In fig. 7, the first cervical ganglion is double. Fr0riep’s ganglion is independent of the rudimentary crest and shows two proximal roots, one connecting With a small lateral spur. The distal root is large and its fibers join the caudal root of the hypoglossal some distance ventral to the spinal cord. Next anterior are three connected masses of ganglion cells which increase in size cephalad. Two proximal and two distal roots are seen‘. The distal roots are extremely small and it is doubtful whether their fibers enter the hypoglossal. Anterior to these three ganglionic masses is a large ganglion elongate in the line of the ganglionic crest. Five groups of proximal roots arise from the myelencephalon and distal roots join the spinal accessory. The anterior of these is the largest. Soon after it unites with the spinal accessory a short very slender cord of cells and fibers passes over to the jugular ganglion (fig. 7, ac). This is the only connection between the hypoglossal ganglia and the jugular ganglion of the vagus.



FIG. 7. Dissection of an 18 mm. pig with three distal roots passing from the hypoglossal ganglia to the ventral roots of the hypoglossal nerve. The first cervi cal ganglion is double and the neural crest is persistent from the first cervical to the jugular ganglion.


The hypoglossal ganglia are best developed in the 17 mm. embryo shown in fig. 6. In this case three distal roots join the hypoglossal from as many ganglia, and a fourth distal spur is present. The first cervical ganglion is only partially divided. Comparing the hypoglossal ganglia with one division of the first cervical ganglion as seen in fig. 4, the resemblance is plain.

From ten dissections at this stage we would note the following points: (1) The hypoglossal ganglia here reach their highest difierentiation; (2) in every case Froriep’s ganglion was present with a well developed hypoglossal root,——in three cases two such hypoglossal roots were present, in one case the ganglion was forked and in one case (fig. 6) there was evidence of four hypoglossal ganglia with distal roots; (3) this stage proves that the connection between the jugular ganglion and the hypoglossal ganglion is of little importance other than showing that both are derived from a common neural crest; (4) as observed in preceding stages, there is great variation in the hypoglossal ganglia of different individuals, and on the two sides of the same embryo; no two were exactly alike; (5) the root of the spinal accessory could be traced back to the eighth cervical ganglion.


Stage 5. 28-30 mm. In succeeding stages the hypoglossal ganglia show retrogressive changes as to structure and relative size. Fig. 8 shows the persistence of a single hypoglossal ganglion (Froriep’s) posteriorly. Anteriorly three closely connected ganglia are seen, the more posterior sending a spur backward, which ends abruptly. This condition was found in two cases. In one case a double hypoglossal ganglion was present, and in one case a small spurred fragment occupied a position near the middle of the hypoglossal chain, that is, about midway between Froriep’s ganglion and the jugular ganglion.

Stage 6. 41-50 mm. Two dissections showed conditions similar to the preceding. A double Froriep’s ganglion was found in one case relatively smaller than in the embryo of 30 mm. Its arrested development was shown by its unchanged position and small size. It lies still partly dorsal to the spinal accessory, while the cervical ganglia have shifted ventrad owing to the elongation of their roots, and to their own growth.


FIG. 8. Dissection of a 28 mm. pig showing Froriep’s ganglion and a distal root to the hypoglossal nerve. The middle portion of the series of hypoglossal ganglia, present in earlier stages, has disappeared.


Theoretical Discussion

It seems evident from the different dissections we have made that the hypoglossal nerve first develops as several ventral spinal roots (5 to 6 in number) which arise independently, lie parallel to each other and are in series with spinal nerves. Later these independent roots unite to form the trunk of the hypoglossal nerve. Comparing the earlier stages with the later, it would seem that the more anterior roots atrophy and this is in harmony with the observations of Bremer (’08).


Allowing that the hypoglossal is a composite of ventral spinal roots, then we should expect to find their ganglia, if present, between the first cervical and jugular ganglia. VVe do find a chain of ganglia occupying this very position, but they are rudimentary, appear late and soon show retrogressive changes. They arise from the same neural crest as do the spinal ganglia and root ganglia of the vagus and glossopharyngeal. They form a continuous series, but show variations in form characteristic of all rudimentary structures. As far as their early development is concerned they cannot be divided into a pre—cervical and a cerebral group, nor is there an overlapping of spinal and cerebral ganglia, according to the theory of Froriep.


Objections have been raised as to whether these ganglia were really homologous with spinal ganglia. The points made have been: (1) Difference in form, these rudiments rarely resembling spinal ganglia; (2) their frequent connection with the vagus rather than with the hypoglossal; (3) their lack of segmental arrangement; (4) their many variations and irregularities of form.


As to their form, in the sheep Froriep found it similar to that of the cervical ganglia. In the pig where they are best developed they are usually spindle-shaped, but broader forms, resembling spinal ganglia, have occasionally been observed. In many mammals too, including man, the first cervical ganglion loses its typical form and may become vestigial. In the pig the first cervical is smaller than the other spinal ganglia and develops later. I have frequently found it double, consisting of two spindleshaped masses of cells. Other spinal ganglia show the same condition. The first cervical ganglion possesses always several proximal roots (4-5) and the distal root arises as two distinct bundles. Froriep’s ganglion never shows more than two proximal roots, generally only one, and never more than one distal root. As these ganglia are also spindle-shaped I would regard them as not homologous with a spinal ganglion, but as comparable to one of the spindle-shaped divisions of such a cervical ganglion as seen in fig. 4. Two of the rudimentary hypoglossal ganglia with their two distal roots would be exactly homologous with a single spinal ganglion. The separation of the two parts of the ganglion could be accounted for as due to their arrested development; as they do not appear until late and the pre—cervical region grows more rapidly, the two masses of cells representing a ganglion would be separated to a greater or less extent. At any rate, we find that the first cervical ganglion is frequently divided in the same way, sometimes the second cervical, and the same thing may occur throughout the spinal series. The irregularities of structure and constant variation which we find in the hypoglossal ganglia is merely typical of all rudimentary structures.


Lewis has objected that the connection of the hypoglossal ganglia with the vagus is more marked than their relation to the hypoglossal. He figures the hypoglossal ganglia (his “beaded commissure”) as continuous with the jugular ganglion. I have shown that the direct connection with the jugular ganglion is only important as showing their common development from the neural crest. Occasionally this connection entirely disappears and it is to be compared to the loops of cells which may persist between the proximal roots of two adjacent spinal ganglia. Furthermore as many as three ganglia may be connected by distal roots with the roots of the hypoglossal. It is my opinion that the anterior ganglia of this series originallyrelated to thehypoglossal, have become connected with the vagus complex, just as in man some fibers from the first cervical ganglion have joined the spinal accessory.


The present lack of segmental arrangement displayed by these ganglia does not preclude their metameric origin. Their development begins considerably later than that of the spinal nerves, and the rapid growth of the region they occupy, before they make their appearance, may cause them to shift their positions with relation to their myotomes. They certainly appear in regular series and their early development is similar to that of the spinal ganglia.

As to the number of dorsal ganglia represented in the hypoglossal series, no absolute statement can be made. The evidence of comparative anatomy goes to show that four or five spinal nerves have been added to the cranial series as a result of the union with the cranium of a corresponding number of vertebrae. Meeks (’09) finds in an Acanthias embryo three rudimentary spinal ganglia located between the vagus and the first spinal nerve, the ganglion of which would correspond to Froriep’s ganglion in mammals. According to this evidence, four dorsal ganglia have become rudimentary structures in mammals and the corresponding ventral roots have united to form the hypoglossal trunk. Regarding each pair of the eight ganglionic nodules found in the 13 mm. embryo as homologous to a single spinal ganglion, then we would have the same number of ganglia, four, represented between the first cervical and the jugular. The more anterior roots of the hypoglossus, which are found in the early embryos but disappear in the later stages, represent ventral roots of the Vagus and glossopharyngeal according to the observations of Bremer (’08).

Conclusions

1. The jugular and superior ganglia of the vagus and glossepharyngeal nerves, the hypoglossal ganglia and ganglia of the spinal nerves arise in the pig embryo from a continuous neural crest, as observed by Streeter in human embryos.

2. The hypoglossal ganglia are retarded in their development, but appear in embryos of 13 mm. as a series of eight connected cell masses of nearly equal size. HYPOGLOSSAL GANGLIA OF PIG EMBRYOS 281

3. According to their development, the hypoglossal ganglia can be divided only artificially into a cephalic cerebral group and a caudal pre—cervical group.

4. The first cervical and other spinal ganglia are often of double origin, composed of two spindle-shaped masses, and generally possess two distal roots.

5. The spindle—shaped ganglion of Froriep with its single distal root would therefore represent but one half of a spinal ganglion.

6. The degree of development of the hypoglossal ganglia varies in different embryos; in the same embryo the right side may be better developed than the left, and vice versa. This is good evidence of their rudimentary or vestigial character.

7. One, frequently two or three, and in one case four hypoglossal ganglia possessed single distal roots and the fibers of three of these joined the hypoglossal nerve.

8. The connection of the hypoglossal ganglia with each other and with the jugular ganglion represents a persistence of the neural crest. It is similar to the connections which were found persisting between the roots of the spinal ganglia.

9. If we consider a pair of hypoglossal ganglia as the equivalent of a single spinal ganglion, four such ganglia would be represented in pig embryos, between the jugular and the first cervical.

10. The hypoglossal trunk develops as five or six separate ventral roots, at first parallel and independent, later uniting to form a single nerve.

11. The hypoglossal ganglia reach their maximum development in embryos 17-20 mm. long, then retrograde, though ganglia at both ends of the series may persist in the adult.

12. The spinal accessory nerve develops very early, being well formed in the youngest embryos examined (5 mm. long). As development proceeds the fibers of the spinal accessory root may be recognized farther and farther caudad. In a pig of 17 mm. a few accessory fibers were traced to a point opposite the eighth cervical ganglion.

References

BREMER, J. L. Aberrant roots and branches of the abducent and hypoglossal 1908. nerves. Jaw. Comp. New‘. and Psych., vol. 18, pp. 619-639, 9 figs.

FRORIEI’, A. Ueber ein Ganglion des Hypoglossus. Archiv f. Anat. u. Physiol., 1882. Anal. Abth., 1882, pp. 279-302.

FRORIEP, A. UND BECK, W. Ueber das Vorkommen dorsaler Hypoglossuswurzeln 1895. mit Ganglien in Reihe der Siiugethiere. Anat. Anz., Bd. 10, pp. 688-696.

LEWIS, F. T. The anatomy of a 12 mm. pig. Amer. Jour. Anat., vol. 2, pp. 2111903. 225, 4 pls.

MARTIN, 1’. Die Entwickelung dcr neunten bis zwéilften Kopfnerven bei der 1891. Katze. Anat. Avn2., Bd. 6.

l\/IEEK, A. The encephalomeres and cranial nerves of an embryo of Acamhias

1909. vulgaris. Anat. Amt, Bd. 34, pp. 473475. STREETER, G. L. The development of the cranial and spinal nerves in the occipi1904. tal region of the human embryo. Amer. Jour. Anat., vol. 4, pp. 83 116, 4 pls.. 14 text figs.


Accepted by the Wistar Institute of Anatomy and Biology, May 16, 1910. Printed September 9, 1910

Explanation of Figures

All drawings were made with the aid of a. camera lucida and have been reduced to a common magnification of about 25 diameters. The figures show in surface view the right side of the myelencephalon and spinal cord from a point antel ior to the origin of the glossopharyngeal nerve to a point just caudad to the first, second or third cervical ganglion. The following abbreviations have been employed:

C1, C2, first and second cervical ganglia; crist. neur., neural crest; gang. Froriep, Froriep’s ganglion; gang. hypogl., hypoglossal ganglia; gang. jugul., jugular ganglion; gang. nodos., ganglion nodosum; gang. petros., ganglion petrosum ; gang. sup., superior ganglion; nod., persisting cellular nodules of neural crest; sp. cord, spinal cord; IX, X, XI, XIII, glossopharyngeal, vagus, spinal accessory and hypoglossal nerves; XI’, peripheral portion of spinal accessory nerve.


Cite this page: Hill, M.A. (2019, September 20) Embryology Paper - The development of the hypoglossal ganglia of pig embryos. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_development_of_the_hypoglossal_ganglia_of_pig_embryos

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