Paper - The roots of the facial nerve in human embryos and fetuses

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Pearson AA. The roots of the facial nerve in human embryos and fetuses. (1947) J Comp Neurol. 87(2):139-159. PMID 20267602.

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This 1947 paper by Pearson describes the development of the facial nerve in embryo and fetal stages.


Also by this author: Pearson AA. The development of the eyelids. Part I. External features. (1980) J. Anat.: 130(1): 33-42. PMID 7364662 PDF
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The Roots of the Facial Nerve in Human Embryos and Fetuses

Anthony A. Pearson

Anatomical Laboratory, University of Oregon, Medical School, Portland

Thirteen figures (1947)

Introduction

The mixed nerves are formed by a combination of elements which develop partly within the central nervous system and partly without. There are many gaps in our knowledge concerning the manner and the sequence in which-these elements unite to form a nerve. Our knowledge is equally limited as to the nature of the functional components within these nerves. This is particularly true of the facial nerve. The main features of the development of the facial motor nuclei have been described in a recent paper (Pearson, ’46). The present account will be limited to a description of the roots of the facial nerve, their connections within the brain stem, and a discussion of the various components within these roots. The peripheral branches of this nerve will be considered in a later paper. Since there are extensive reviews of our knowledge on the facial nerve in the literature (Ariiéns Kappers, Huber and Crosby, ’36; Vraa-Jensen, ’42), only references pertinent to the observations described in the present paper will be cited.

This report is based on the study of serial sections of human embryos and fetuses prepared with the various silver techniques. These stains include pyridine silver, Bodian and a more recently developed method, the silve1:'-gelatin stain (Pearson and O’Neill, ’46; and Pearson, ’47). The estimated age of the embryos and fetuses studied is based on the crownrump length and the data given recently by Patten (’46).


Description

The portion of the facial nerve which has its origin outside of the central nervous system is derived partly from the aeoustico-facial ganglion. This ganglion is originally a single mass of cells which lies close to the auditory vesicle. At an early period, the cell mass which becomes the geniculate ganglion of the facial nerve, begins to separate from the side of the acoustico-facial ganglion (Streeter, ’12). This separation of the geniculate ganglion from the acoustic portion of the original ganglionic mass is a gradual process. A stream of cells can be seen between the 2 masses of cells in embryos where the separation has not been complete. A portion of the facial nerve ganglion is often left behind in the internal auditory meatus in close relation to the vestibular portion of the acoustic ganglion (fig. 1). This may be seen as a cluster of cells or simply as scattered cells among the fibers of the VII nerve. These cells remain among the fibers of the VII nerve within the internal auditory meatus and develop into large ganglion cells similar to those in the genieulate ganglion.

Abbreviations

a, fiber layer beneath floor of fourth ventricle

b.v., blood vessel

dec.VII, decnssation or crossed fibers of facial nerve

(l.r.V, descending root of trigeminal nerve

fas.so1., fasciculus solitarius

f.mo.r.VII, fibers of motor root of VII

f.N.int., fibers of ncrvus internu-dius

f.I\'.V, fibers of trigeminal nerve

f.VII, or f.N.VII, fibers of facial nerve

g:mg.gen., or gen.gan., geniculate ganglion

gang.ves., vestibular ganglion

genu VII, genu of facial nerve

in.gang.VII, inner part of ganglion of facial nerve

int.aud.me., internal auditory nneatus

mo.nu.V, motor nucleus of trigcminal nerve

mo.r.V, motor root of trigeminal nerve

mo.r.VII, motor root of facial nerve

N.coc., cochlear nerve

N.int., nervus intermedius

N.ves., vestibular nerve

N.VI, abducens nerve

N.VII, facial nerve

N .VIII, acoustic nerve

nu.ac.VII, accessory nucleus of facial nerve

nu.coc., cochlear nucleus

nu.fas.sol., nucleus of faS('l('1ll1lS solitarius

nu.r.d.V, nucleus of descending root of V

nu.VI, nucleus of abduct-ns nerve

nu.VII, nucleus of facial nerve

pre.VII nu.fas.sol., pr:-facial portion of nucleus of fasciculus solitarius

semi.can., semicircular canal


In the older fetuses they are easily distinguished from the small bipolar cells in the vestibular ganglion. Occasionally there is a communicating branch between the vestibular ganglion and the portion of the facial nerve within the internal auditory meatus. This would indicate that fibers of the facial nerve may either follow the vestibular nerve for a part of its course, or that they join the VIII nerve.


Fig. 1 A cross section through the brain stem of a 10-week (46-mm CR) human fetus (no. 22) showing the path of the facial nerve through the internal auditory meatus. Bodian stain (section 29-1-4).

The majority of the fibers of the facial nerve when traced centrad through the internal auditory meatus can be followed into the large motor root. When an inner part of the facial nerve ganglion is present, part of the VII nerve fibers can be traced here. The facial nerve fibers which enter the brain between the motor root of VII a.nd the acoustic nerve constitute the nervus intermedius (fig. 2). Sometimes the fibers of nervus intermedius tend to be collected into a compact bundle which follows the Ventral border of the vestibular nerve a11d its ganglion (fig. 3). More often the fibers of nervus intermedius are grouped in a number of smaller bundles which enter the brain stem in separate fascicles. Frequently a small bundle of VII can be traced caudal to these and was found to enter the medulla oblongata at a lower level. This rootlet could easily be mistaken in cross sections of the brain stem for one of the more rostral rootlets of the glossopharyngeal nerve.


Fig. 2 A cross soctiml through the brain stem of :1 10 week (46-mnl CR) human fetus (no. 22) showing the relations of the nervus intcrmcdius to the vestibular and the facial norws. Bodian preparation (section 29-1-2).


Fig. 3 A cross section through the brain stem of a 10-week (47-mm CR) human fetus (no. 101) showing the relationship of the nervus iutermedius to the VII and the V111 nerves. Bodian preparation (section 21-1-2). X 19.


Fig. 4 A cross section through the brain stem of an 11-week (65n1m CR) human fetus (no. 80) showing parts of the VII and the VIII nerves. Note the fibers of nervus intermedius which extend toward the midlinc. Pyridine silver preparation (section 41-2-3). X 20.

As the fibers of the nervus intermedius sink deeply into the medulla oblongata, the majority of them pass through the descending root of the trigeminal nerve and its nucleus. Some of these fibers of the nervus intermedius are lost among the fibers and the nucleus of the descending root of V. The termination of some of the fibers of nervus intermedius within the nucleus of the descending root of V has been recognized by a number of authors and is now accepted as a fact.


The more dorsally placed fibers of the nervus intermedius enter the medulla oblongata close under the fibers of the vestibular nerve, and they follow this nerve in a dorsomedial direction until they reach the faseieulus solitarius (figs. 4, 5). Many of them enter the ventrolateral aspect of this bundle. The majority of the fibers of the facial nerve which join the fascieulus solitarius appear to descend with the fibers of this bundle. But a few of these fibers are thought to ascend in a portion of the fasciculus which lies rostral to the roots of the facial nerve. Their failure to show up in the Marchi preparations of experimental animals (Allen, ’23) would suggest that these fibers are either unmyelinated or only lightly myelinated. A few of the facial nerve fibers which ascend are thought to join the caudal end of the meseneephalic tract of V. This connection is best shown in the sagittal sections of embryos stained with pyridine silver.


Fig. 5 A portion of :1 cross section of the brain stem of :1 12-week (80 mm (,‘-R) human fetus (no. 83) showing the relation of the nervus intermedius to the vestiluular nerve. Pyridine silver preparation (section 69-2-2).


At the level of the most rostral bundle of the nervus intermedius, the nucleus of fasciculus solitarius is seen as a rounded mass of small poorly staining cells (fig. 5). It lies ventral to the vestibular nuclei and dorsal or dorsomedial to the nucleus of the descending root of the trigeminal nerve. In this position the solitary nucleus can be traced rostrally into a position lateral to the dorsal portion of the motor nucleus of the V nerve (fig. 6). It rostral end lies lateral to fibers which continue into the caudal end of the mesencephalic tract of V. This rostral extension will be referred to as the prefacial portion of nucleus of fasciculus solitarius. The prefacial portion of the nucleus of the fasciculus solitarius is not surrounded by or in relation to a conspicuous group of fibers as is often the case with more caudal portions of this fasciculus. In fact fibers do not make up a conspicuous part of the rostral end of this system, and because of this, the prefaeial portion is often obscured by the fibers of the surrounding areas. Accordingly it does not stand out as distinctly in the adult brain as it does in the fetus.


Fig. 6 A portion of a cross section of the brain stem of a 12-week (80mm CR) human fetus (no. 83) at the level of the motor nucleus of the trigcminal nerve. Note the prcfacial portion of the nucleus of fasciculus solitarius. Pyridine silver preparation (section 67-1-1).


Only part of the fibers of the nervus intermedius which penetrate deeply into the brain stem enter the faseieulus solitarius. A portion of them continue toward the midplane, passing either rostral or dorsal to the abducens nucleus. Here they join the main motor component of the facial nerve and are lost among its fibers (figs. 4, 7). These fibers may be part of a main bundle of the nervus intermedius to faseiculus solitarius or they may be in smaller and less conspicuous bundles which pass between the solitary fasciculus and the main motor root of VII. These fibers of the nervus intermedius which continue toward the midplane are more conspicuous in certain fetuses than in others. This is thought to be due to the fact that they are grouped into more compact bundles in certain specimens.


Fig. 7 A cross section of the brain stem of a 10-week (45 mm CR) human fetus (no. 91) at the level of the genu of the facial nerve. Note the fibers of the motor root of VII on the right side and on the left side the fibers of nerrus intermedius which extend toward the midline. Pyridine silver preparation (section :31 2-2). X 22.


While the main facts regarding the path of the motor fibers of VII around the abducens nucleus are well known, certain points need to be restated. The majority of the fibers from the chief motor nucleus of VII course in a dorsomedial direction toward the caudal pole of the abducens nucleus. They are seen as scattered fibers or in very small bundles. Unless the tilt of the sections and the staining are favorable, they will more than likely remain unobserved. Some of these fibers pass around the caudal pole of the abducens nucleus, other fibers pass around its medial border, and still others pass directly through this nucleus to reach its medial side. Here the fibers of VII collect in a compact bundle just beneath the floor of the fourth ventricle. This bundle ascends in this position to about the level of the rostral pole of the abducens nucleus. Here its fibers turn laterally, then ventrolaterally, and course toward the ventrolateral surface of the brain stem in a broad curve. They pass lateral to the motor nuclei of VII and medial to the nucleus of the descending root of V. On reaching the surface of the brain stem they pass directly into the internal auditory meatus Where they are_ joined by the fibers of nervus intermedius.


The fibers in the facial genu which turn laterally at the rostral pole of the abducens nucleus, form part of a layer of fibers which lies just beneath the floor of the fourth ventricle (fig. 8). This layer is complex in that its fibers are derived from a number of sources. The more rostral part of the layer contains motor fibers of the trigeminal nerve which pass toward the midplane, and the more caudal portion contains fibers of the facial nerve. When the fibers of this layer are followed toward the midplane, many of them will be observed to cross to the opposite side. Not all of the motor fibers of the facial nerve take the path through its internal genu. Many of them, on approaching the midplane, join the layer of fibers just beneath the floor of the fourth ventricle. Some of these fibers cross to the other side and there become part of the fiber layer (figs. 7-10). They are thought to contribute to the facial nerve of the opposite side.


Fig. 8 A cross section of the brain stem of a, 10-week (45-mm CR) human fetus (no. 91) at the level of the genu of the facial nerve. The level is slightly rostral to that of figure 7. The letter :1 dosignzltes a layer of fibers beneath the floor of the fourth ventricle. Pyridine silver prepm-:1tion (section 22-2-2 . X 22.


Fig. 9 A diagrunl drawn from cross sections of the brain stem of an 11-week (65 mm C-lt) human fetus (no. 80), showing parts of the course of the facial norw. Fmm p)'ridine silver preparations (slide 41). X 20.


Fig. 10 A portion of a cross section of the brain stem of :1 7-month (255-nnn CR) human fetus (no. 96) at the level of the germ of the facial nerve. Note the erased fibers of VII. Pyridine silver preparation (section 61-2-1). X 26.


Fig. 11 A cross section through the brain stem of a newborn tuiencephalic baby (no. 95) at the level of the VI and VII nerves. Pyridine‘ silver proparation (section 31-2-3). X 35.


Wth regard to this crossed connection, the brain stem of an anencephalic baby is of interest (figs. 11, 12). In this specimen the chief motor nucleus of VII is divided into 2 main groups. There is a caudal group whose fibers take the usual course in the genu around the abducens nucleus and turn laterally at the rostral pole of that nucleus (fig. 11). A large part of the VII nerve in this specimen takes its origin from a group of cells rostral to the level of the VI nucleus (fig. 12). These fibers do not take the path through the internal genu. Many of them course do1'somediall_v to about the position of the accessory facial nucleus and then turn laterally. These fibers join the facial nerve of the same side. A number of fibers, however, continue toward the midplane a11d many of them cross to the other side. The brain stem of this anencephalic baby extends rostral to the facial nerve level for only a short distance. Only a portion of the VIII nerve complex is present. The field is thus not complicated by the large number of fibers which cross the field in a normal brain stem. In this respect it is almost like an experimental animal. It was not possible to determine Whether or not the fibers of the accessory facial nucleus were among these crossed fibers.



Fig. 12 A cross section through the brain stem of a newborn aneneephalie baby (no. 93) at the level of the V11 nerve. The level of the section is slightly rostral to that of figure 11. A rostral group of cells of the nucleus of VII occurs at this level. Pyridine silver preparation (section 31-4-3). X 35.


Fig. 13 A photomicrograph of a section through the motor root of the facial nerve of an 11-week (65-mm CR) human fetus (no. 80). Note the spindle shaped swellings which occur on some of the fibers of VII just proximal to their place of exit from the brain stem. Pyridine silver preparation ‘(section 42-1-2).


Small bipolar cell—like structures sometimes occur in the motor root of the facial nerve (fie: 13). These are best shown in our pyridine silver preparations in fetuses of 3 to 5 months of age. They are concentrated in the portion of the motor root just central to. its place of exit from the brain stem. They usually stain quite darkly and this makes the recognition of nuclei difficult. A few of them are more lightly stained and appear to contain a nucleus. Our failure to find these structures more regularly within fetal brains, however, raises some doubt as to whether these actually are neurons.

Discussion

The relations of the roots of the facial nerve in the human fetus are very similar to those found in lower mammals. The most dorsal fibers of the nervus intermedius commonly lie close under the vestibular nerve. A portion of these fibers continue toward the midplane in a number of animals. Lorente de N6 (’33) shows the relations of this bundle in the mouse in his figure 44 and labelled it X3. He thought it belonged to the autonomic system. Addens (’34) and Kimmel (’41) identified this connection in the rabbit. Addens considered it to be crossed salivary fibers of VII. Ramon y Cajal (’09), Shaner (’34) and others have thought these fibers to be a component of the vestibular nerve. The course of this component of nervus intermedius resembles that described for the crossed limb of the olivary peduncle of Papez (’30) and Rasmussen (’-16). The fibers of the olivary peduncle were thought to arise from cells in the region of the superior olive, to cross the midplane near the abducens nucleus, and to leave the brain stem in close company with the vestibular nerve. The peripheral distribution of this bundle, however, was thought to be with the acoustic nerve rather than with the facial nerve.


In our material it was not possible to trace these fibers of the nervus intermedius definitely across the midplane or to determine the location of their cells of origin. The relations of this bundle to the vestibular nerve in some series were so intimate that it could not be traced as a distinct bundle into the facial nerve. In several series of human fetuses, however, it was possible to trace it definitely into the facial nerve. This does not necessarily rule out the possibility of the existence of fibers which take the course described for the olivary peduncle and which distribute with the acoustic nerve to part of the membranous labyrinth.


The visceral afferent fibers of the nervus intermedius enter the rostral portion of the fasciculus solitarius. The majority of these fibers turn eaudalward, but a few of them turn rostralward. These ascending fibers are thought to be the result of the bifurcation of some VII nerve fibers on entering the solitary fasciculus, as is the case with a portion of the fibers of the IX and the X nerves. This is in agreement with Herrick (’44) who describes a prefacial portion of fasciculus solitarius in Amblystoma. Herrick has described it as being more slender and less well myelinated than the caudal portion of that fasciculus. The fact that it is smaller and less well myelinated than the part of the fasciculus caudal to the level of entrance of VII many explain why it has been usually overlooked.


It is generally believed that the more caudal portions of the fa sciculus solitarius are concerned with general visceral sensibility, and that the centers for taste are at the levels of the entrance of the fibers VII, IX and X into the solitary fasciculus or in the rostral end of the nucleus of fasciculus solitarius. This would suggest that the prefacial portion may be primarily a center for taste. It is well known that while taste buds develop on the anterior two-thirds of the tongue, very few taste buds are present in this region in adult man (Ariens Kappers, Huber and Crosby, ’36). This would indicate that only a few fibers in the VII nerve of the adult are concerned with taste conduction and may account for the fact that the prefacial portion of the nucleus of fasciculus solitarius is much more prominent in the fetus than it is in the adult.


Larsell and Fenton ( ’28) have identified a cutaneous auricular branch of VII in the human fetus whose cells of origin were thought to be in the geniculate ganglion. This branch is similar to the cutaneous branch of VII described in the mouse by Rhinehart (’18). The consensus is that these cutaneous fibers of VII terminate within the brain stem in the nucleus of the descending tract of V. fibers accompanying the mesencephalic tract of V have been traced caudad as far as the roots of the VII and the VIII nerves in Amblystoma (Herrick, ’14). Kimmel (’41) made a similar observation in rabbit embryos. He found these fibers to divide, one process joining the facial nerve and the other passing to the facial motor nucleus. The caudal extension of the fibers accompanying the mesencephalie tract of V to the level of the VII and the VIII nerves can be confirmed in our sagittal series of human embryos, together with the fibers in VII which join the mesencephalie tract of V. It seems highly probable that these fibers constitute a small proprioceptive component in the facial nerve. Degeneration experiments have revealed that 7% of the fibers in the facial nerve, just distal to the stylomastoid foramen, remain after cutting the roots of this nerve central to the geniculate ganglion (VI-Iakeley and Edgeworth, ’33). The conclusion drawn was that the facial muscles have an afl’erent nerve supply through VII. Van Buskirk (’45), however, failed to find fibers in nervus intermedius which he considered to be large enough to be within the size range for the conduction of muscle sense. He states that they fall well within the range of cutaneous fibers.


Certain authors have claimed the presence of fibers within the facial nerve which are concerned with the conduction of pain (Hunt, ’15, ’37; Davis, ’23; Bruesch, ’44). Others have denied the existences of pain fibers within VII (Carmichael and Woollard, ’33; and others). If there are pain fibers within the VII nerve, they probably terminate along with the other cutaneous fibers of VII in the nucleus of the descending root of V.


Early in the development of the human embryo the motor nucleus of the facial nerve differentiates from a column of cells which lies close to the midplane. Axons grow out from these cells and form the motor root of VII. Streeter (’08) has described how the abdueens nucleus migrates rostralward, pushing before it the motor fibers of VII. The cells of the facial motor nucleus migrate ill a ventrolateral direction, thus forming the internal genu of that nerve. The abducens nucleus seems to act as anchor for the bend of the genu. Neurobiotactic influences similar to those which are thought to be responsible for the migration of the abducens nucleus a11d motor nucleus of VII may very likely pull some motor neuroblasts of VII across the midplane at a very early period. This would account for a crossed component in VII.


A number of investigators have claimed the presence of crossed fibers in the facial nerve (Barker, 1899; Ramon y Cajal, ’09; Obersteiner, ’01; and others). Almost as many authors have denied the existence of a crossed component in VII (Van Grehuchten, ’06; Papez, ’27; and others). Windle’s (’33) photographs of sections of cat embryos showing the decussation of facial nerve fibers are very convincing. In older fetuses and in the adult brain stem there are so many fibers crossing the field at this level that the crossed fibers of VII are diflicult to follow with certainty. These crossed fibers of VII could be seen much more clearly in the brain stem of an anencephalic baby than in a normal brain. There seems little to support Vraa—Jensen’s (’42) suggestion that the crossed fibers of the facial nerve arise in the lateral reticular nucleus. Some of these crossed fibers may correspond to fibers in the olivary peduncle which has been discussed earlier in this paper (see p. 152).


The possible clinical significance of a crossed component in the facial nerve has been discussed in a recent paper (Pearson, ’46). It seems likely that the upper facial muscles receive an innervation from the motor facial nuclei of both sides, while the lower facial muscles receive their innervation only from the same side. This may explain why the lower facial muscles of one side are often paralyzed without any involvement of the upper facial muscles.


Van Buskirk ( ’45) has estimated that 58% of the fibers of the facial nerve in man are special visceral efferent, 24% are general visceral efierent, and 18% are sensory. He found the number of nerve fibers peripheral to the geniculate ganglion to be greater than that central to the ganglion, the increase being over 1300 fibers. This would suggest the presence of autonomic ganglion cells within the geniculate ganglion, since it is generally recognized that there are more postganglionic fibers leading away from an autonomic ganglion than there are preganglionic fibers leading into it. Van Buskirk (’45), however, failed to find any autonomic ganglion cells in the geniculate ganglia in his series. He suggests that the nerve fibers may branch in the region of the ganglion, or that the great superficial petrosal nerve may send fibers into the facial nerve. In the older fetuses in our series‘ the geniculate ganglion is composed of large cells which are somewhat variable in size. So far we have not been able to determine the exact character of all of its cells.


One might expect to find several nuclei giving rise to the general visceral elferent fibers of the facial nerve: one for the innervation of the submaxillary and sublingual glands, another for the innervation of the lacrimal gland, and perhaps a third for the innervation of the glands in the mucous membranes of the nose and the roof of the mouth. A number of authors have pointed out various groups of cells which they considered to be the source of these autonomic fibers. The evidence, however, has not been too convincing. The general visceral motor cell column of the vagus and glossopharyngeal nerves does not extend up to the level of nervus intermedius. The evidence while not complete, suggests that the source of these fibers may either lie closer to the midplane or even on the opposite side. This View is supported by the experiments of Wang (’42) on cats. A reactive region for the stimulation of flow of saliva from the submaxillary gland was found in the region of the facial genu. Another possibility is that they may come from the scattered cells, lying medial to the fasciculus solitarius and not from any well defined group or groups of cells.


There is very little evidence to support the suggestion that the cells of the accessory nucleus of VII are the source of general visceral efferent fibers. They resemble more closely the special visceral motor cells of V and VII (Pearson, ’46).


The suggestion has been made that these cells send their fibers to the phylogenetically older muscles innervated by VII,_which include the stylohyoid, posterior belly of the digastric, and the stapedius muscles (Strong and Elwyn, ’43).

There is still much to be learned about the anatomy and physiology of the facial nerve. A careful study of the development of the peripheral pattern of its branches and their connections should contribute to the further analysis of this nerve.

Summary

At an early period in human development the geniculate ganglion is formed by a separation of cells from the acousticafacial ganglion. Some of the ganglion cells often remain in the path of the facial nerve within the internal auditory meatus. These cells constitute a second ganglion of variable size. In the older fetuses the size of these cells and their position among the fibers of the VII nerve distinguish them from the cells of the vestibular ganglion.


The fibers of the nervus intermedius usually enter the brain stem grouped in a number of small fascicles, rather than in a single bundle. The fibers of the nervus intermedius have the following distribution within the brain stem. Some of its fibers end in the nucleus of the descending root of V. These fibers are thought to be concerned with the conduction of cutaneous sensations. The Visceral afferent fibers enter the rostral portion of the fasciculus solitarius. While the majority of these fibers descend, a few are thought to ascend. The few proprioceptive fibers within the VII nerve are thought to enter the caudal end of the mesencephalic tract of V. Some of the fibers of nervus intermedius continue medial to the fasciculus solitarius and extend toward the midplane. These fibers are lost among the fibers which make up the genu of VII. The sources of the general visceral motor fibers is still a matter of speculation.


The nucleus of fasciculus solitarius extends rostral to the level of the facial nerve as high as the motor nucleus of V.


The rostral extension of this cell column is referred to as the prefacial portion of the nucleus of fasciculus solitarius.


The development of the course of the special visceral motor fibers of the VII nerve through the internal genu is followed in human embryos and fetuses. The author is in agreement with certain of the earlier neurologists in that part of the motor fibers of the facial nerve are crossed. Observation on the brain stems of abnormal specimens support this view. The presence of crossed fibers in the VII nerve is thought to be of clinical significance.

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Cite this page: Hill, M.A. (2019, May 25) Embryology Paper - The roots of the facial nerve in human embryos and fetuses. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_roots_of_the_facial_nerve_in_human_embryos_and_fetuses

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