Paper - The hypoglossal nerve in human embryos (1939)
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The Hypoglossal Nerve In Human Embryos
Anthony A. Pearson
Loyola Unyiversity, School of Medicine, Chicago, Illinois
This paper is the second in a series of studies on the development and analysis of the cranial nerve components in human embryos. These studies were made on serial sections of human embryos cut in different planes and stained by various methods. The methods used in preparing the embryos have been given in a previous paper (Pearson, ’38).
The human embryos referred to speciﬁcally in this paper are listed below with certain necessary data.
Human crown rump length Probable age ' Method of embryo no. in millimeters in weeks preparation H. 1360 17 7 Pyridine silver H. 1194 25 8 Pyridine silver 15 42 10 Activated protargol 4 43 10 Activated protargol 21 45 10 Activated protargol 22 46 10 Activated protargol
Human embryos nos. H. 1360 and H. 1194 belong to the collection of Prof. Gr. W. Bartelmez of The University of Chicago. The others listed are in the author’s collection. The activated protargol method was used according to the procedure described by Bodian (’37).
The author is grateful to Prof. E. C. Crosby for extending him the privileges of the Anatomical Laboratory of the University of Michigan during the summer of 1938, and for the use of two series of adult human brain stems stained with toluidin blue. The author is indebted also to Prof. G. W. Bartelmez of The University of Chicago and Prof. Davenport Hooker of the University of Pittsburgh for the use of several series in their embryological collections.
Since the literature on the comparative anatomy of the XII cranial nerve has been summarized by Mingazzini (’28), and Aliens Kappers, Huber and Crosby (’36), only references pertinent to this discussion will be mentioned here.
Nucleus Of Origin
Streeter (’08) has shown that the motor elements in the brain stem of a 10 mm. human embryo form a continuous column which extends from the spinal cord into the medulla oblongata. A longitudinal division has divided this column into a medial and a lateral column. The hypoglossal nucleus of Stilling (1843) differentiates from the medial column.
In human embryos of 25 mm. CR length, the hypoglossal nucleus is still seen as a prolongation of the cervical anterior gray column into the medulla oblongata (ﬁg. 6). These two regions fuse without sharply delimiting landmarks. The characteristic cell groupings present in later development cannot be distinguished.
In older stages showing the early development of the pyramids and their decussation, the continuation of the hypoglossal cell column with the anterior horn of the spinal cord is less evident. The nucleus of the XII nerve is situated on either side of the median raphe close under the ependyma, and extends from about the level of the highest root of the X nerve to a plane passing a little below the obex. The length of this nucleus is a little less than that of the inferior olive. The constituent cells are large multipolar neurons in various stages of development. None of these neurons, however, have reached the size seen in the adult brain.
In human fetuses of 45 mm. or more CR length, the hypoglossal cell column shows-a division into a dorsal and a ventral cell column. Nearly all of the cell groups present in the adult are indicated; however, all of these groups have not as yet completely differentiated.
The dorsal cell column occurs through the greater part of the length of the XII nucleus and extends farther cephalad than the ventral column. The ventral cell column in turn extends a little farther caudad and is located approximately in the caudal two-thirds of the XII nucleus. The cephalic end of the dorsal column has become divisible into a medial and a lateral part (figs. 1 and 2). The medial part is situated dorsomedial to the somewhat smaller lateral part. The two are bounded, medially by the nucleus eminentia medialis (or nucleus eminentia teres); dorsally by vthe. ependyma and nucleus intercalatus. On tracing these parts caudad, the nucleus eminentia medialis (fig. 1) soon disappears, and gradually the nucleus intercalatus grows smaller and changes from a dorsolateral to a more dorsal position with respect to the hypoglossal nucleus. The medial and the lateral parts of the XII nucleus also become smaller. A little past the midpoint of the hypoglossal cell column the two fuse thus forming a single cell mass. This cell mass forms the caudal end of the dorsal column which drops out a little before reaching the caudal limit of the XII nucleus.
a, ﬁbers turning forward out of ramus descendens and into the XII nerve
a.carot.ex., arteria carotis externa
a. carot. int., arteria carotis interna
a. ling., arteria lingualis
a. vert., arteria vertebralis
b, sympathetic nerve ﬁbers accompanying the lingual artery
01, first cervical nerve
can. hyp., canalis hypoglossi
c.thyr., cartilago thyreoidea
fas. sol., fasciculus solitarius
gang. C1, ganglion of the first cervical nerve
gang. C2, ganglion of the cervical nerve
gang. C3, ganglion of the third cervical nerve
gang. cerv. sup., ' ganglion cervicale superius trunci sympathici
gang. nod. N.‘ X, ganglion nodosum nervi vagi
med.obI., medulla oblongata m.geniogl., musculus genioglossus m.geniohy., musculus geniohyoideus m.hyogl., musculus hyoglossus
m. mylohy., musculus mylohyoideus
n1. stylogl., musculus styloglossus
m. thyreohy., musculus thyreohyoideus
n amb., nucleus ambiguus
n. d. mo. X, dorsal motor nucleus of X
11. em. med., nucleus exninentia medialis
n.inter., nucleus intercalatus
n. oliv., nucleus olivaris inferior
N.IX, nervus glossopharyngeus
N.X., nervus vagus
N .XII, nervus hypoglossus
n. XII, nucleus nervi hypoglossi
n.XII d, dorsal group of the ventral column of the hypoglossal nucleus
11. XII 1, lateral group of the dorsal column of the hypoglossal nucleus
11. XII m, medial group of the dorsal column of the hypoglossal nucleus
n.XII v, ventral group of the ventral column of the hypoglossal nucleus
os hyoid., os hyoideum
os. occ., os occipitale
r. desc., ramus descendens nervi hypoglossi
sp. cord, spinal cord
submax. g1., submaxillary gland
v. jug. int., vena jugularis interna
Fig.1 A cross section through the medulla oblongata of a human embryo (no. 22) at the level of the rostral end of the hypoglossal nucleus. Activated protargol preparation (section 37-24). .>( 20.
Fig. 2 A cross section through the medulla oblongata of the same embryo at a level 9. little in front of the middle of the hypoglossal nucleu. Activated protargol preparation (section 41-2~1). ‘X 20.
In the adult brain the dorsal column of the hypoglossal nucleus is divisible into two groups which extend through the whole length of that column. A third group is also present at certain levels near the cephalic end of the column.
Fig.3 A cross section through the medulla oblongata at a level near the caudal end of the XII nuclear column. Human embryo no. 22. Activated protargol preparation (section 45-1-1). )< 20.
At about one~third of the length of the hypoglossal nucleus from its cephalic end, the ventral column of cells gradually enters the ﬁeld ventral to the dorsal cell column, and extends caudally to a little below the level of the obex, where it is lost. The ventral column in turn is divisible into two parts, a larger dorsal part and a smaller ventral part (ﬁg. 2). The ventral part of the ventral column is less well deﬁned. It is com— posed of darkly staining large multipolar cells situated among the root ﬁbers of XII and along the ventral border of the dorsal part of the ventral column. A characteristic section in this region will show several of these cells in this position.
The dorsal part forms the main group of the ventral column (fig. 3) which extends farther caudad than the other cell groups of the hypoglossal nucleus.
The more general relations of the XII nucleus in the human brain stem have been given by Sabin ( ’01)’ and Weed (’14), but without a. consideration of its various cell groups.
There have been a number of studies on lower animals, based on normal and experimental material, attempting to determine speciﬁc centers within the hypoglossal cell column for the various tongue muscles (Koska and J agita, ’03; Stuurman, ’16; and Berkelbach van der Sprenkel, ’24). Human clinical‘materia1 has also been used in trying to work out a localization pattern within the XII nucleus (Parhon and Papinian, ’04; Goldstein and Minea, ’09; and others). The conclusions are not in complete agreement and it is diﬁicult to evaluate the ﬁndings.
Contrary to the statements in at number of the current text books of anatomy, many investigators believe that the nucleus for the ﬁbers innervating the geniohyoid muscle is located in the medulla oblongata within the hypoglossal nucleus. A phylogenetic study of the nuclear groups of the XII nerve is in progress at the University of Michigan. Only a preliminary report of this work has now been published (Barnard, ’37). Since the material under consideration throws no additional light on the question, the localization problem will not be discussed here.
Along the ventral border of the hypoglossal nucleus there is a group of small cells which are not clearly delimited from the surrounding reticular gray substance. This nucleus is poorly developed in the stages studied but it probably corresponds to the cell group known as Roller’s nucleus (Ramon y Cajal, ’09). In this material no evidence was observed that these cells contribute ﬁbers to the roots of XII.
There is a small group of closely packed small cells located medial to the ventral column of the hypoglossal nucleus at about the level of the junction of the caudal and middle thirds of the XII nucleus. This group of cells is not always at exactly the same level as the corresponding group on the opposite side. An additional group of such cells may be in much the same position, but a little farther rostralward. This may correspond to the nucleus described by Schwentker (’27) in the adult human brain. It was not possible to trace the processes from these cells.
Fig.4 A composite diagrammatic representation of the course of the XII x_\erve as it may be followed in the cross sections of a human embryo (no. 22). From activated protargol preparations.
The nucleus intercalatus (of Staderini, 1895) is somewhat cone—shaped, with its large end directed forward (ﬁgs. 1 and 2). It lies parallel to, and in close relation with, the XII cell column, the two forming a slight bulge in the ﬂoor of the fourth ventricle known as the trigonum hypoglossi. The caudal end tapers off and extends as a narrow strand of small cells along the dorsal border of the XII nucleus, but thickens again toward its caudal pole. Sagittal series reveal that this is a continuous strand of cells. The nucleus intercalatus is thought by most observers to contribute no ﬁbers to the roots of XII.
Course of the Nerve
Root ﬁbers collect in small bundles along the ventral border of the XII nucleus (ﬁgs. 4, 6, and 7). These bundles course ventrad and slightly late1'ad, and enter the hilus of the in ferior olive. Instead of coursing directly through the olive, they turn slightly mediad, cutting through the ventral olivary wall, and leave the medulla oblongata lateral to the developing pyramid. The ﬁbers arising from the caudal end of the hypoglossal cell column cross the medullary ﬁeld in a more nearly straight line.
After leaving the medulla oblongata, the root ﬁbers of XII are easily followed. They gradually converge into larger bundles, and passing dorsally of the vertebral artery, course ventrolaterad. These bundles unite farther into two or three bundles, usually two, and make their exit from the cranial cavity through the hypoglossal canal. According to Streeter (’04) the hypoglossal nerve has originated through the fusion of three or four segmental spinal nerves which have been enclosed within the cranium. Bremer (’08) reported that it is not uncommon to ﬁnd ﬁbers continuing the line of ventral roots between the XII and the VI cranial nerves.
The roots of XII fuse as they leave the cranial cavity and pass toward the vagus nerve. The XII nerve may ﬁrst come in contact with the X nerve either in the region of the ganglion nodosum or a little above that ganglion. As XII courses around the nodose ganglion, it may lie either in close contact with the ganglion or it may occupy a groove in the ganglion, and thus be in a more intimate relationship with the vagus nerve. XII then passes ventrad between the internal jugular and the internal carotid, and in the region of the posterior border of the developing hyoid bone it gives off a branch which runs caudad to supply the thyrohyoideus muscle. The nerve continues ventrad and slightly cephalad forming an arch with its convex border below. It passes medial to the stylohyoid muscle and the submaxillary gland, and lateral to the lingual artery and the hyoglossus muscle. In the root of the tongue branches of the nerve are given off to the hyoglossus muscle. The XII nerve passes above the geniohyoid muscle, which it supplies with branches, and turns mediad in front of the hyoglossus muscle to enter the tongue. The hypoglossal nerve passes through the genioglossus muscle and into the body of the tongue, where it breaks up into its terminal branches and innervates both the intrinsic and the extrinsic muscles of the tongue.
The trunk of the hypoglossal nerve is made up chieﬂy of medium and large-sized medullated nerve ﬁbers. There are a few nonmedullated nerve fibers in the spaces between the medullated ﬁbers (in the cat, dog and rabbit, Koch, ’16, and in the cat, Langworthy (’24 a). In adult. animals no unmyelinated nerve ﬁbers were observed within the roots of XII.
The hypoglossal nerve receives, during its course a number of communicating branches. One of these is a very delicate ﬁlament which runs with XII as that nerve passestthrough the hypoglossal foramen. Peripherally this ﬁlament becomes lost in the loose connective tissue in the region of the carotid plexus. It was not possible to follow the course of these ﬁbers centrally to the foramen.
Soon after leaving the hypoglossal canal, the XII nerve receives a small ﬁlament from the ﬁrst cervical nerve. This ﬁlament appears to run centrad with XII. Its termination is undetermined and its signiﬁcance not understood. At the point of origin of this ﬁlament from the ﬁrst cervical nerve there is a group of cells resembling a small ganglion.
The XII nerve is sometimes joined by a communicating branch from the superior cervical ganglion or the sympathetic trunk just before XII comes in contact with X.
The hypoglossal nerve receives a root from the anterior ramus of the ﬁrst cervical nerve which in turn has received a branch from the anterior ramus of the second cervical nerve (ﬁgs. 5, 6 and 7). This communicating branch from the first and second cervical nerves joins XII just as that nerve arches around the border of the ganglion nodosum. Here XII is in intimate relationship with X and the ganglion nodosum. To what degree there may be an exchange of ﬁbers is difficult to determine in this material.
The ramus deseendens leaves XII as the latter passes forward from the ganglion nodosum. Berkelbach van der Sprenkel (’24) considers that in the hedgehog, ﬁbers from the second cervical dorsal root ganglion ascend in the ramus deseendens hypoglossi and turn forward with XII. This appears to be the case in certain human ernrbyos. This relation is more easily observed in younger embryos (ﬁgs. 5, 6, 8 and 9) than in older fetuses.
Streeter ( ’04) found in many human embryos that the connections of the hypoglossal nerve with the upper cervical roots are coincident with, or precede the appearance of the ramus deseendens (XII). In some cases however, the ramus deseendens developed before receiving branches from the cervical nerves. Streeter also pointd out that the early arrangement of the root ﬁbers of XII and the upper cervical nerves resembles the spokes of a wheel, being perpendicular to the neural tube. Thus, adjacent ﬁbers are bound together at the time their sheaths are formed. As would be expected, a certain amount of variation is found in the arrangement of the communicating branches of the upper cervical nerves with XII and the ramus descendens. Streeter considered that the character of ramus descendens is dependent on the nature of the contributions from the cervical nerves. He pointed out however, that ﬁbers destined for the descending ramus may be picked up either with the more caudal roots of the XII nerve, which will result in little or no communication between the hypoglossal nerve and the first cervical nerve or these ﬁbers may be picked up with the ﬁrst cervical nerve, course with the XII nerve for a short distance, and then proceed to their destination.
Fig.5 A composite semischematic drawing showing the form of the ansa hypoglossi in 9. young human embryo of about 7 weeks. Note the proximity of the mouth and the heart in an embryo of this age. Human embryo no. H. 1360. From pyridine silver preparations out in the sagittal plane.
Goldstein and Minea (’09) concluded that the descending ramus of XII in man does not take its origin from the hypoglossal nucleus, but from the cervical cord. Stuurman (’16) found no degeneration in the XII nucleus after the removal of the ramus descendens in the mouse.
The descendens cervicalis is formed by branches from the anterior rami of the second and third cervical nerves. The ansa hypoglossi has already been formed in all of the embryos studied. In the younger stages studied, this loop is very hort. Thus it is easy to understand how cervical ﬁbers may ascend in the ramus descendens (ﬁg. 5). It is in older stages where the structures in the neck have enlarged and separated farther, that the relations resembling those in the adult are found.
Fig. 6 A drawing similar to the preceding ﬁgure illustrating the coure of the XII nerve in a human embryo of about 8 weeks. The hypoglosal nucleus is seen as a prolongation of the cervical gray column into the medulla oblongata. Human embryo no. H. 1194. From pyridine silver preparations cut in the sagittal plane.
After X.II crosses the lateral surface of the hyoglossus muscle, it turns around the anterior border of that muscle and is joined by a small ﬁlament of ﬁbers which accompanies the lingual artery (ﬁg. 4). These ﬁbers can be traced back along the lingual artery and into the carotid plexus.
In the tongue, the XII nerve receives a communicating branch from the lingual nerve.
Fig.7 A composite diagrammatic drawing showing the origin, course, and distribution of the hypoglossal nerve in a human embryo of about 10 weeks. From activated protargol preparations cut in the sagittal plane. Human embryo no. 21.
In the root of the tongue, the XII nerve occasionally communicates with its fellow on the opposite side. This was observed in two human fetuses (no. 4 and 15). In each case the communicating branch ran in front of the hyoid bone and between the genioglossus and the geniohyoid muscles.
Andersch called this branch the transverse arch (Scarpa, 1794).
A Sensory Component
Froriep (1882) found in certain hoofed animals persistent dorsal roots and ganglia associated with the caudal rootlets of the hypoglossal nerve. Similar hypoglossal ganglia have been described in other forms and referred to as Froriep’s ganglia. The presence of such ganglia in relation to the hypoglossal nerve in man is considered extremely rare. In many human embryos there is a small ganglionic swelling on the trunk of the spinal accessory nerve a little above the ganglion of the ﬁrst cervical nerve. In none of the material studied does this ganglion appear to have a direct connection with the hypoglossal nerve. This ganglion is probably one of the accessory root ganglia (Pearson, ’38).
Fig. 8 A drawing of a sagittal section through the junction of the hypoglossal nerve and ramus descendens (see fig. 6). This ﬁgure shows ﬁbers from the descending ramus turning forward with the hypoglossal nerve. Human embryo no. H. 1194. Pyridine silver preparation (section 15-2-2). X 225.
It may be true that remnants of tlie dorsal root ganglia of the segmental nerves which have become incorporated into the hypoglassal nerve are included among the more caudal accessory root ganglia. Their axons, instead of passing directly to join XII, may follow the accessory root ﬁbers to the Vagus nerve and possibly join XII as the latter hooks around the ganglion nodosum. Langworthy (’24 b) concluded on the basis of the chromatolytic changes in experimental material that some of the sensory ﬁbers in XII have their cells of origin in the nodose ganglion of X.
Fig. 9 A photomicrograph of the section drawn in the preceding figure. Some of the ﬁbers shown in the drawing are out of focus in this picture. X 225.
It has been pointed out that in one of the human embryos studied, there are ﬁbers in the descendens hypoglossi which turn forward with the XII nerve (ﬁgs. 8 and 9). This agrees with Berkelbach van der Sprenkel (’24), who described in the hedgehog sensory ﬁbers in the XII nerve Whose cells of origin are located in the ganglion of the second cervical nerve. That author considered that some of the ﬁbers which ascend in the ramus descendens XII, innervate for muscle sense the thyrohyoideus, the hyoglossus, and the styloglossus muscles.
Sherrington (1894) has described the XII nerve in an amyelous fetus, whose central nervous system had been destroyed by some pathological condition after the neural crests had developed. In this specimen the XII nerve appeared to be formed largely by a branch from the second cervical ganglion and a branch from the vagus nerve below its ganglion. In the tongue the XII nerve gave off branches to the tongue muscles.
Corbin, Lhamon and Petit (’37) have described in the rhesus monkey a small number of degenerating ﬁbers in the distal portion of the hypoglossal nerve after the removal of the second cervical dorsal root ganglion. These authors suggested that there is an extracranial contribution of sensory ﬁbers to the XII nerve from the second cervical dorsal root ganglion. This contribution was regarded as probaby proprioceptive in nature. It was further suggested, that the relation of XII and the upper cervical nerves in the monkey may be different from that in the eat, Where XII Was thought to contain no ﬁbers which originate in the upper cervical dorsal root ganglia (Hinsey and Corbin, ’34). However, the experiments of Langworthy (’24 b) on cats would indicate that XII receives proprioceptive ﬁbers not only from Froriep’s ganglion, but also the second cervical dorsal root ganglion and the ganglion of X. In these experiments, Langworthy found that the neuromuscular spindles disappeared from the tongue muscles after cutting the XII nerve, and concluded that the hypoglossal nerve carries proprioceptive ﬁbers. The degeneration experiments of Yee, Harrison and Corbin (’39) on the rabbit, revealed that a small contribution (1 to 5%) of sensory ﬁbers from the dorsal root ganglion of the ﬁrst cervical nerve joins the peripheral portion of the XII cranial nerve.
In the work of Tarkhan (’36) on cats and dogs, it was found that stimulation of the central stump of XII caused an increase in arterial pressure and reﬂex movements of the jaw and tongue. Barron ( ’36) however, found no evidence of proprioceptive impulses in the XII nerve.
It is of interest to mention the work of Olmstead and Pinger (’36), who found that the XII nerve, when sutured to the lingual nerve, can initiate the regeneration of taste buds in the papillae where they have disappeared as a result of cutting the lingual nerves.
Muscle spindles have been observed in the tongue of man and many other animals by a number of authors (Hinsey, ’34, and others) which would indicate a proprioceptive innervation.
More work will be necessary, however, to establish the validity of a sensory component in XII. The evidence at hand would suggest that proprioceptive ﬁbers join the hypoglossal nerve, and that their cells of origin are probably located in the dorsal root ganglia. of the upper cervical nerves and possibly the nodose ganglion.
The hypoglossal nerve has been shown to arise from a column of cells which is seen as a prolongation of the anterior gray column of the cervical spinal cord into the medulla oblongata.
The hypoglossal cell column differentiates into a. dorsal and a ventral column. The dorsal column in turn is divisible into a medial and a lateral group. A third group may appear later. The Ventral column becomes divided into a dorsal and a ventral group. A group of small cells was observed which may correspond to the group described by Schwentker (’27).
The course of the XII nerve and its relations in the embryos studied are described. The XII nerve was found to have communicating branches which connect it with the ﬁrst and second cervical nerves, the superior cervical sympathetic ganglion or the sympathetic trunk, the carotid plexus, and the lingual nerve. In a few cases the hypoglossal nerve was observed to send a communicating branch to itsifellow on the opposite side.
Fibers have been observed in the descendens hypoglossi which turn forward with XII. This would indicate that upper cervical spinal nerve ﬁbers course with the hypoglossal nerve. These ﬁbers may be proprioceptive.
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