Paper - The development of the nervus terminali in man

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Pearson AA. The spinal accessory nerve in human embryos. (1938) J. Comp. Neurol. 68(2): 243-266.

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This historic 1941 paper by Pearson described development of the nervus terminali.


See also by this author: Pearson AA. The spinal accessory nerve in human embryos. (1938) J. Comp. Neurol. 68(2): 243-266. Pearson AA. The hypoglossal nerve in human embryos. (1939) J. Comp. Neurol. 71(1): 21-39. Pearson AA. The development of the olfactory nerve in man. (1941) J. Comp. Neurol. 199-217. Pearson AA. The trochlear nerve in human fetuses. (1943) J. Comp. Neurol. : 29-43. Pearson AA. The oculomotor nucleus in the human fetus. (1944) J. Comp. Neurol. 47-.
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The Development of the Nervus Terminalis in Man

Anthony A. Pearson

Loyola University, School Of Medicine, Chicago, Illinois

Twenty-One Figures (1941)

Introduction

It is within relatively recent times that the first account of the nervus terminalis in mammals was published (DeVries, ’05). There still remains a great deal to be learned concerning its development, connections and function. The early literature dealing with the nervus terminalis has been summarized by Johnston ( ’13) and Larsell (’18). Mention should be made that this nerve was figured first in a selachian by Fritsch (1878), and later described in another fish, Protopterns, by Pinkus (1895). This nerve was referred to as the nerve of Pinkus for a number of years. After extensive studies based on selachians, Locy (’O5) suggested the name “nervus terminalis”. This term has been in general use since that time. Johnston (’13) concluded that the nervus terminalis exists in addition to the vomeronasal nerve and that it consists of a ganglionated nerve whose roots enter the telencephalon caudal to the olfactory bulb. Huber and Guild (’13) prepared rabbit embryos in which the nervus terminalis was differentially stained. They found that the nervus terminalis is an independent nerve whose peripheral course is through a loose plexus. Groups of ganglion cells were observed along the course of the nerve and the largest of these was considered to be the ganglion terminale. Some of the fibers of the nervus terminalis follow the course of the vomeronasal nerve and others are distributed to the septal mucosa anterior to the path of the vomeronasal nerve. McCotter (’15) dissected the nervus terminalis in the human fetus and infant, and found the peripheral course of the nerve similar to that described for the rabbit. Simonetta (’32) is in agreement wih MeCotter with regard to the general structural plan of the nervus terminalis in human embryos. Brookover (’14) and Johnston (’14) have described the intracranial course of the nervus terminalis in adult man as lying over the surface of the gyrus rectus and the entrance of the nerve into the brain as being in the region of the medial olfactory striae.

The development of the nervus terminalis is so intimately related to the development of the olfactory and the vomeronasal nerves that it is difi‘ieult toidescribe one without some reference to the other two. A study of the development of the olfactory nerve will be published at a later date (Pearson, ’41). These papers are part of a research program devoted to the study of the development and the analysis of the cranial nerve components in human embryos. The observations recorded here were made on the serial sections of human embryos cut in different planes and stained by various methods. The methods of preparation have been given in a previous paper (Pearson, ’38).

The human embryos referred to specifically in this paper are listed on the following page with certain necessary data.

GANGLION TERMINALE

The ganglion terminale and the nervus terminalis could not be distinguished in a 9 mm. human embryo stained with copper protargol. It is evident that the nervus terminalis develops soon after this stage of development for the anlage of the ganglion of this nerve is easily recognizable in a 14 mm. human embryo. This is in agreement with the observations of J ohns— ton (’13). It is clear that important changes take place in the formation of the nervus terminalis and its ganglion during the sixth and seventh weeks of human development.

Bianchi (’31) has described the early development of the so-called “olfactory ganglion” and its relation to the development of the nervus terminalis in the guinea pig. According

HUMAN GROWN-RUM? LENGTH PROBABLE AGE METHOD OF EMBRYO NO. IN MILLINIETEIR-S IN WEE-KS PREPARATION E 204 9 5% Copper protargol (Bodian) B 808 14 6 Copper protargol 16 17 7 Pyridine silver 48 17 7 Copper protargol W 712 20 7 % Pyridine silver 31 22 % Copper protargol W 820 23 8 Pyridine silver W 781 24 8% Pyridine silver B 1194 25 2}; Pyridine silver W 743 26 8:} Pyridine silver 27 29 9 Copper protargol 29 29 9 Copper protargol 30 38 10 Copper protargol 2 38 10 Pyridine silver W 701 45 11 Pyridine silver 21 45 11 Copper protargol 22 46 11 Copper protargol VV 660 47 11 Pyridine silver 45 78 13 Copper protargol

The letter, “W” indicates the embryos that belong in the collection of Professor W. F. Windle of Northwestern University; “B” indicates those that are in the collection of Professor G. W. Bartelmez of The University of Chicago. The 9 mm. human embryo belongs to the collection of Professor Martin Essenberg of Loyola University. The others listed are in the author ’s collection. The author gratefully acknowledges his indebtedness to Professors Windle, Bartelmez, and Essenberg.

to this author, the “olfactory ganglion” comes from the epithelium of the olfactory fossa. The nervus terminalis in the guinea pig also originates from the olfactory placode, not directly, but secondarily from the differentiation of the ganglion elements in the “olfactory ganglion”. Bianchi pointed out that the “olfactory ganglion” is not properly named in that it contains some elements which are destined to constitute the ganglion of the nervus terminalis and are thus not part of the olfactory nerve. Simonetta (’32) recognized two parts in the so-called “olfactory ganglion” of human embryos; a medial part (the ganglion terminale) which contains cells resembling neuroblasts, and a lateral part (the olfactory por tion) containing small cells. The ganglion cells of the nervus terminalis in the rat (Stewart, ’20) are derived from the proliferation of cells from the septal portion of the olfactory sac.

The ganglion terminale and the vomeronasal nerve in the human embryo arise from the medial border of the olfactory placode (fig. 1). It is this region of the olfactory placode which gives rise to the Vomeronasal organ. The cells which constitute the ganglion terminale in a 14 mm. human embryo form

ABBREVIATIONS

a. N. te1'm., anterior septal branch of nervus terminalis

bulb. olf., bulbus olfactorius

bulb. o1f.acc., bulbus olfactorius accessorius

f, fibers of nervus terminalis

fila olf., fila olfactoria

f. N. term., fibers of nervus terminalis

ga11g.cel1, ganglion cell

gang. et N. term., ganglion terminale et nervus terminalis

gang. term., ganglion terminale

hyp., hypophysis

lam. fib., lamina fibrarum nervi olfactorii

med. nasal process, median nasal process

N. ant. eth. (N.V), anterior ethmoidal nerve (a. branch of the trigeminal nerve)

nasal epi., nasal epithelium

N. nasop-al., branch of the nervus nascpalatinus

N. o1f., nervus olfactorius

N. ’cerm., nervus terminalis

N. term. et N. vn., nervus terminalis et nervus vomeronasalis

N. vn., nervus vomeronasalis

r. N. term., root or roots of nervus terminalis

v., ventriculus

vn.o., vomeronasal organ


“maxillary process

«’..med. nasal process

Fig.1 A transverse section through the head of a 14 mm. human embryo (no. B. 808). Copper protargol preparation (section 14-3-7). X 25.

irregular masses along the medial side of tlie olfactory nerve. It is not possible in many of these younger embryos to diiferentiate between the elements of the nervus terminalis and those of the vomeronasal nerve. The olfactory nerve fibers arise from the dorsal region of the placode just lateral to the anlage of the vomeronasal organ. The term, “olfactory ganglion”, will not be used in referring to the mass of nerve fibers and sheath cells which constitute the olfactory nerve at this stage of development. N o ganglion cells were observed among its fibers and it is not thought to be a true ganglion. It will be referred to simply as the “olfactory nerve”.


Fig. 2 A transverse section through the forebrain of a 20 mm. human embryo (no. W 712). Pyrid.ine silver preparation (section 16-3~2). X 34.

The olfactory nerve in the sagittal sections of embryos of about 17 mm. (nos. 16 and 48) is seen as a broad band of cells and fibers stretching between the dorsal surface of the olfactory placode and the wall of the forebrain. There are groups of cells which stain differentially from the surrounding mesoderm situated medial to the olfactory nerve. These groups are connected by strands of cells with the medial border of the olfactory placode and constitute the ganglion terminale at this stage of development. No fibers of the nervus terminalis could be followed into the brain in these preparations of 17 mm. human embryos.

The olfactory nerve in a 20 mm. human embryo consists of an irregular mass of cells (sheath) and fibers (fig. 2). At this stage of development the ganglion terminale is close against the olfactory nerve. The ganglion may be distinguished by the many darkly impregnated fibers among its cells. A sharp boundary line between the two does not exist. This close relationship of the ganglion terminale with the olfactory nerve extends dorsally along the medial border of the latter to the region of the junction of the olfactory nerve with the wall of


Fig.3 A sagittal section through the forebrain of a 22 mm. human embryo (no. 31). The level of the section is just medial to the developing olfactory bulb. Note the relation of ganglion terminale to the forebrain. Copper protargol prepa~ ration (section 14-13). ‘x 51.

the forebrain. Here the ganglion terminale appears to be fused with the Wall of the forebrain. The vomeronasal nerve is without doubt present in the lateral part of the complex of fibers and cells which constitutes the ganglion terminale. The ganglion terminale (fig. 3) is well shown in the sagittal series of a 22 mm. human embryo. One end of the ganglion tapers slightly as it extends toward the ventral wall of the forebrain. At the place of junction of the ganglion with the wall of the forebrain, the external limiting membrane of the brain has disappeared. This allows the fibers of the ganglion terminale to continue into the forebrain. There are many cells among the fibers of the nervus terminalis in the region of its entrance into the forebrain. These cells form a continuous stream from the forebrain out into the body of the ganglion where the cells are more densely placed. This suggests that there is a migration of cells from the brain out into the ganglion. A similar situation has been described in the turtle (Larsell, ’19). These cells resemble the migratory cells in the ventral roots of the spinal nerves of turtle embryos (Kuntz, ’11) and of chick embryos (Jones, ’37). The distal end of the ganglion shows an irregular enlargement which breaks up into a number of branches. The ganglion terminale lies along the medial border of the olfactory nerve. The two structures look almost continuous in places; however, a fairly distinct line marks the boundary. In the region where the two structures fuse with the forebrain, a small blood vessel runs between them.


The nervus terminalis is sometimes less well developed in one embryo than in others of the same estimated age. This would suggest a certain amount of variation in the rate of development of this nerve and its ganglion. An example of this is a human embryo of 29 mm. (no. 27). The ganglion terminale in this embryo is distinctly less well developed than in other human embryos of a comparable age. This aspect of the developmental history of the nervus terminalis will not be emphasized in order to present a more logical sequence of events.


The ganglion terminale in human embryo no. W 820 (23 mm.) has begun to separate from the olfactory nerve (fig. 4). The ganglion appears to be more clearly defined on the left side of the figure than on the right. This illustrates that there is also some variation in the arrangement of the fibers and in the grouping of the cells. The caudal part of the ganglion terminale in this embryo still lies close against the ventramedial wall of the forebrain (fig. 5, left).


The olfactory system shows further development in a 24 mm. human embryo (fig. 6). The lateral margin of the ganglion terminale is still in close relation to the olfactory nerve. The caudal end of the ganglion has begun to separate from the


Fig. 4 A transverse section through the forebrain of a 23 mm. human embryo (110. W 820). Pyridine silver preparations (section 17-2-6). X 34.


Fig. 5 A transverse section through the forebrain of a 23 mm. human embryo (no. W 820). The level of the section is a little caudal to that of the preceding figure. The left side of the figure is a little rostral to the right side. Pyridine silver preparation (section 17-1-3). .X 34.


ventromedial wall of the forebrain. Many cellular elements are present among the fibers of the nervus terminalis where they enter the brain. The ganglion terminale shows further signs of separation from the wall_ of the forebrain in a 25 mm. human embryo. The ganglion is no longer connected with the forebrain except for the central roots of the nervus terminalis whose course lies over the surface of the olfactory nerve (figs. 7 and 8). In human embryos of about 29 mm. (nos. 29 and 27) the olfactory bulb has begun to enlarge. The ganglion terminale is seen as an irregular mass of cells and fibers medial to the border of the developing olfactory bulb.


Fig.6 A transverse view through the forebrain of a 24 mm. human embryo (no. W 781). Pyridine silver preparation (the left half of the figure is from section 34-1-2 and the right half from sections 32-1 5 and 6). X 30.


In a 38-mm. human embryo (no. 30) the ganglion terminale is situated close to the layer of olfactory nerve fibers of the medial wall of the olfactory bulb (fig. 9). The majority of the fibers of the olfactory fila may be traced into the bulb a little below the level of the ganglion terminale. The ganglion at this age is still a fairly compact mass of cells and fibers. The course of the nervus terminalis caudad to its place of entrance into the brain lies close to an area which is thought to be the accessory olfactory bulb (or formation). The vomeronasal nerve in a number of lower forms has been traced to the accessory olfactory bulb (McCotter, ’12). Humphrey ( ’40) has made a similar observation in human fetuses. As the fibers from the ganglion terminale are followed cauded in this embryo, fiber bundles turn laterad to enter the bulb in the region of the accessory olfactory bulb. These fibers are considered to be part of the vomeronasal nerve. The remaining fiber bundles may be traced farther caudad to enter the forebrain behind the accessory olfactory bulb. A few of these fibers turned rostrad into the accessory olfactory bulb. This would indicate that some of these fibers are a part of the vomeronasal nerve. The remaining fibers which enter the brain caudad to the accessory olfactory bulb are thought to belong to the nervus terminalis. The plane of the sections of an embryo may not always be favorable for distinguishing the central roots of the vomeronasal nerve from those of the nervus terminalis. In a number of embryos studied the central roots of the vomeronasal nerve are difficult to follow and it is easy to understand how DeVries (705) and Dollken (’09) failed to recognize that there were two nerves and not one in the vomeronasal and terminalis nerve complex. Recently Humphrey (’40) has made a more complete study of the accessory olfactory bulb and the reader is referred to her paper for further details.


Fig. 7 A sagittal section through the head of a 25 mm. human embryo (no. B 1194). The section is medial to the olfactory bulb. Note the ganglion terminale and the course of a few fibers of the nervus terminalis within the brain. Pyridine silver preparation (section 24-2-2). X 34.


The olfactory bulb is a conspicuous structure in embryos of 10 and 11 Weeks (fie: 10). The ganglion terminale and the olfactory bulb in series W 701 (45 mm.) are two rather distinct structures. This is particularly true in pyridine silver preparations where there is often a selectivity of the stain for the fibers of the nervus terminalis. The fibers of the nervus terminalis in this human embryo are well impregnated with silver, while the fibers of the olfactory and the Vomeronasal nerves are very lightly stained.


Fig. 8 A sagittal section through the head of a. 25 mm. human embryo (no. B 1194) at the level of the developing olfactory bulb. This section illustrates the close relation of the olfactory nerve and the nervus terminalis at this stage of development. Pyridine silver preparation (section 25»2-3). X 34.



Fig.9 A composite drawing made from several consecutive cross sections through the forebrain of a 38 mm. human embryo (no. 30). Copper protargol preparation (slide 17). X 34.


Fig. 10 A diagrammatic representation of the peripheral course of the nervus terminalis as it may be followed in the sagittal sections of a 45 mm. human embryo (no. 21). From copper protargol preparations. Approximately X 13.

The sagittal series of a 45 mm. human embryo (no. 21) was favorable for the study of the ganglion terminale. The anterior septal branch of the nervus terminalis enters the rostral end of the ganglion. The branches of the vomeronasal nerve and the branches of the nervus terminalis which accompany this nerve enter the ventral border of the ganglion terminale (fig. 10). The ganglion is seen as a network of interlacing fibers with many groups of ganglion cells among the fibers. Fiber bundles collect at the caudal border of the ganglion and may be traced to the base of the olfactory bulb where they enter the forebrain. The central roots of the nervus terminalis in this specimen branch and anastomose.


In series no. 22 (46 mm.) the mass of fibers and cells which constitute the ganglion terminale extends forward from the region medial to the rostral end of the olfactory bulb and into the region over the cribriform plate. The fibers of the nervus terminalis are not difierentially stained in the material prepared With copper protargol and thus do not stand out in contrast to the fibers of the olfactory and of the vomeronasal nerves. The fibers of the nervus terminalis enter the rostral and ventral sides of the ganglion terminale and are indistinguishable from the fibers of the vomeronasal nerve that pass into the ganglion. Many fibers can be seen leaving the ganglion terminale to enter the medial wall of the olfactory bulb, a little below the accessory olfactory bulb. Other bundles may be traced farther caudad to enter the forebrain just caudal to the accessory olfactory bulb. The latter are the central roots of the nervus terminalis.


The relation of the ganglion terminale to the olfactory bulb is well shown in series no. W 660 (47 mm.). The pyridine silver does not appear to" be as selective for the nervus terminalis in this embryo as in some of the previously mentioned series. The olfactory bulb in older embryos is much larger, but the ganglion terminale and its central roots have not increased appreciably in size and by comparison are smaller (figs. 11 and 12). With further development the ganglion terminale is carried farther away from the forebrain. In a 78 mm. human embryo the ganglion terminale is seen as a loose mass of fibers and cells in the region medial to the rostral end of the olfactory bulb (fig. 13).


It has not been possible to determine the exact shape and character of many nerve cells along the course of the nervus terminalis. The round and oval cell bodies of developing neurons were observed among the fibers of both the ganglion terminale and the peripheral branches of the nervus terminalis. In some embryos it was not possible to distinguish ganglion cells from sheath cells. Along the branches of the nerve peripheral to the ganglion, bipolar and unipolar cells were demonstrated (figs. 14 and 15). A few multipolar cells were seen in the main ganglion. The true morphology of the majority of the cells was not clear.


Fig. 11 A transverse section through th-e forebrain of a 47 mm. human embryo (no. W 660) illustrating the relation of the ganglion terminale to the olfactory bulb. Pyridine silver preparation (section 65-1-1). .X 25.


Johnston (’13) reported the presence of bipolar cells in the ganglion terminale of aipig embryo. Huber and Guild (’13) found that the groups of ganglion cells in the course of the nervus terminalis in the rabbit resemble sympathetic ganglion cells. The last mentioned authors pointed out the difficulty in determining the definite character of the neurons composing the ganglia associated with the nervus terminalis. Unipolar and bipolar cells were observed by Brookover (’17) in the nervus terminalis in an infant. He pointed out that there were 1500 ganglion cells along the peripheral course of the nerve in addition to the many cells in the ganglion terminale. Larsell (’18) has described unipolar, bipolar, and multipolar cells in the nervus terminalis of the cat. A more complete study should be made of the finer structure of these cells in older human fetuses.


Fig. 12 A transverse section through the forebrain of a 47 mm. human embryo (no. W 660). The level of the section (62-1-1) is a little caudal to that of the preceding figure. Pyridine silver preparation. X 25.


Fig. 13 A diagram similar to figure 10 showing the peripheral course of the nervus terminalis in a 78 mm. human embryo (no. 45). From copper protargol preparations. Approximately ‘X 10.


Central Course of Nerve

The central course of the fibers of the nervus terminalis is not easily followed in the very young embryos at my disposal. However, many fibers from the ganglion terminale may be traced into the forebrain in a 20 mm. human embryo (fig. 2). The fibers are grouped in large and small bundles and even layers. Some of the fiber bundles turn mediad and others turn laterad. These fibers are soon lost after they enter the brain.


In a 23 mm. human embryo the caudal end of the ganglion terminale still lies close against the wall of the forebrain. From this end of the ganglion terminale about six small bundles of fibers run caudad to enter the telencephalon (fig. 5, right). The course of these fibers within the forebrain is not well shown. A number of fibers of the nervus terminalis probably enter the brain where the ganglion lies close against the wall of the forebrain (figs. 4 and 5, left). It is diificult to determine what percentage of fibers enters here, or what path these fibers take within the brain. The ganglion terminale in a 24 mm. human embryo still lies close against the olfactory nerve. The fibers of the nervus terminalis course in a broad stream of fibers dorsad and caudad toward the base of the developing olfactory bulb. In addition to the large bundle shown in figure 6, there are some small bundles of the nervus terminalis that enter the brain farther lateralward. The fibers of the nervus terminalis on entering the brain spread out in a fan-like arrangement and are soon lost. The picture is much the same in a 25 mm. human embryo (no. 1194). This series reveals a large stream of fibers passing from the ganglion terminale toward the base of the olfactory bulb (figs. 7 and 8).


Fig. 14 A careful drawing of a section through one of the large branches of the vomeronasal nerve. The heavy dark lines represent fibers of nervus terminalis which accompany the vomeronasal nerve. The right end of the figure is directed toward the brain. From a 45 mm. human embryo (no. W 701). Pyridine silver preparation (section 64»2-3).


Many of these fibers can be traced caudad in the brain for a short distance, but they are soon lost.

A sagittal series of a 38 mm. human embryo (no. 2) reveals a large root extending eaudad from the ganglion terminale to enter the forebrain just caudal to the olfactory bulb. The fibers sink deep into the brain substance (fig. 16). Some fibers continue dorsad into the septal area of the brain while others course in a more caudal direction toward the hypothalamus. They soon disappear and their ultimate termination is not known. A central root of the nervus terminalis in another 38 mm. human embryo (no. 30) is shown in figure 9. The path of these fibers within the brain could not be followed for any great distance. The relation of the nervus terminalis to the central roots of the vomeronasal nerve has already been discussed (see p. 48).


Fig. 15 This illustrates some of the nerve elements observed in the epithelium lining the anterior border of the nasal cavity in a 45 mm. human embryo (no. 21). Two of the nerve cells appear to have migrated out of the epithelium. From a sagittal section (37-2-2) stained with copper protargol.


About six bundles of nerve fibers constitute the central roots of the nervus terminalis in embryo no. W 701 (45 mm.). These bundles may be traced caudad from the caudal end of the ganglion terminale close along the medial surface of the olfactory bulb (figs. 17 and 18). A few fibers tend to mix with the lightly stained olfactory nerve fibers which enter the medial side of the olfactory bulb. The central roots of the nervus terminalis are arranged in a dorsoventral position along the medial side of the olfactory bulb. They enter the ventromedial surface of the forebrain (fig. 19) just caudal to the attachment of the olfactory bulb. The smaller and more ventrally placed bundles enter the wall of the forebrain more laterally. These fibers penetrate deeply into the brain, some turning mediad, some laterad, and others penetrate more deeply into the forebrain, almost at right angles to the surface of the brain. The more dorsally situated bundles are usually larger. These enter the brain in a more medial position. After entering the brain, these bundles take a path close to the medial surface of the brain and may be followed into the septal area (figs. 20 and 21). In this position they break up into small bundles among the cells of the medial septal nucleus. Some of the fibers may end here and others turn laterad into the lateral septal nucleus. The position of the septal nuclei has been given by Hines (’22, see fig. 42).


Fig. 16 A sagittal section through the forebrain of 38 mm. human embryo (no. 2). A root of nervus terminalis is shown entering the brain just caudal to the olfactory bulb. Pyridine silver preparation (a combination of two sections, 14-2-2 and 14-3-2). .X 34.


The central roots of the nervus terminalis are longer in older embryos. This is to be expected as the ganglion terminale is farther removed from the place of the attachment of its roots to the brain. The central roots of this nerve in a 78 mm. human fetus are collected into one main bundle which extends along the medial side of the olfactory bulb ‘(fig. 13).


Peripheral Course of the Nerve

The nervus terminalis is often differentially stained in pyridine silver preparations. In series no. VV 701 (45 mm.) the olfactory and the vomeronasal nerves are poorly impregnated with the silver, but the fibers of the nervus terminalis are darkly stained. This makes it possible to follow the main course of the nervus terminalis with some degree of certainty.


Fig. 17 A transverse section through the forebrain of a 45 mm. human embryo (no. W 701). Pyridine silver preparation (section 63-1-4). X 25.

It may be that the alkaline fixative used in pyridine silver methods results in a more selective staining of certain nervous elements, while the slightly acid fixation of the formol acetic alcohol used before the copper protargol results in a more uniform stain. The state of preservation, the degree of mye— lination, and the age of the embryo may be important factors also.

Several bundles of fibers of the nervus terminalis can be followed from the ventral border of the ganglion terminale through the cribriform plate in company with the branches of the vomeronasal nerve. The dark fibers of the nervus terminalis stand out in contrast to the light stain of the vomeronasal nerve fibers (fig. 14). These dark fibers may be traced along the branches of the vomeronasal nerve toward the vomeronasal organ. They gradually disappear as the vomeronasal organ is approached. It is difficult to determine their exact termination. The path of the branches of the nervus terminalis through the cribriform plate and through the mucous membrane of the nasal septum is usually deep (medial) to most of the olfactory nerve bundles. In the copper protargol material, it is evident that some of the more caudally placed bundles of the nervus terminalis, which follow the branches of the vomeronasal nerve, pass through the cribriform plate in company with bundles of the olfactory nerve.


Fig. 18 A transverse section through the forebrain of a 45 mm. human embryo (no. W 701). The level of the section is slightly caudal to that of the preceding figure. Pyridine silver preparation (section 60-2-5). X 25.


An examination of the cells around the vomeronasal organ leaves little doubt that there is a considerable migration of sheath cells and nerve cells from this source. This migration of cells from the vomeronasal organ evidently continues over a considerable period of time. These migratory cells are prominent around the vomeronasal organ in a 78 mm. human fetus. These cells are often arranged in clusters and chains around the nerve fibers that supply the vomeronasal organ. These nerve fibers are from three sources; the vomeronasal nerve, the nervus terminalis, and the nasopalatine branch of the trigeminal nerve (fig. 10).


A division of the nervus terminalis which is distributed to the anterior septal region arises from the rostral end of the ganglion terminale. This branch is formed by one or ‘two fiber bundles which pass through the cribriform plate to enter the rostral part of the nasal septum (fig. 10). These fibers of the nervus terminalis spread out into a loose network of fine fibers deep to the fila olfactoria. Huber and Guild (’13) referred to the network in the rabbit as the anterior septal plexus. The groups of ganglion cells in this plexus reminded them of the enteric plexus. This plexus is well shown in the sagittal series of older embryos stained with copper protargol. A number of small blood vessels pass through this region but, in the embryos studied, these fibers do not follow or have any particular arrangement with reference to these vessels. The ultimate termination of the majority of these fibers is difficult to determine. As one traces them from section to section, they become less prominent and finally disappear.


Fig. 19 A transverse section through the forebrain of a 45 mm. human embryo (W 701). The level of the section is just caudal to the olfactory bulb. Several of the roots of the nervus terminalis are shown. Pyridine silver preparation (section 58—14). .x 25.


Some of the most rostral fiber bundles of the anterior septal branch of the nervus terminalis distribute to the epithelium of the anterior part of the nasal septum. Nerve cells can be seen in the pseudostratified epithelium of this region. These are like typical olfactory cells. They are bipolar cells with their cell bodies in the epithelium. The peripheral process of each extends outward to the outer margin of the epithelium. Its central process is directed backward toward the olfactory bulb. There are bipolar cells also whose cell bodies are located deep to the epithelium (fig. 15). Their peripheral processes extend through the epithelium to its outer margin and their central processes may be traced centrad with the most rostral fibers of the anterior septal branch of the nervus terminalis. These cells are fusiform, darkly staining, bipolar cells with a small amount of cytoplasm around the nucleus. A nucleolus is usually Visible in the pa.le stippled nucleus. The position of the nerve cells within the epithelium and of the nerve cells close to the epithelium indicates a migration of neuronal elements from the nasal epithelium even in embryos of 10 and 11 weeks. This migration is thought to explain the presence of the many ganglion cells scattered along the more rostral branches of the nervus terminalis. It should be pointed out that some of these fibers which arise from nerve cells in the epithelium of the nasal septum may be olfactory nerve fibers. These fibers may simply course with the most rostral branches of the nervus terminalis and pass through the ganglion terminale to enter the medial wall of the olfactory bulb. There are fibers which leave _the ganglion terminale to enter the medial wall of the olfactory bulb. Coghill (’30) has found that in larval Amblystoma, fibers of the nervus terminalis arise from cells in the olfactory epithelium and enter the brain.


Fig. 20 A transverse section through the forebrain of a 45 mm. human embryo (110. W 701). The level of the section is a little caudal to that of the preceding figure. A portion of the course of the nervus terminalis within the brain is shown. Pyridine silver preparation (section 56-1-1). ,)< 25.


Fig. 21 Another section through the forebrain of the same human embryo (110. W 701). This illustrates further the course of the nervus terminalis within the brain. The level of the section is still farther caudad. Pyridine silver (section 54~2-5). X 25.


The medial nasal branch of the anterior ethmoidal nerve (of V) enters the mucous membrane of the nasal cavity and usually joins the anterior septal branch of the nervus terminalis just under the cribriform plate (McCotter, ’15). These fibers often run with this division of the nervus terminalis for some distance. Their ultimate termination was not shown in this material. Branches of the nasopalatine nerve extend forward in the nasal septum to the vomeronasal organ (fig. 10). These branches from the nasopalatine nerve anastomose with branches of the nervus terminalis in the infant (Brook over, ’17).


Discussion

A few of the earlier investigators considered that the nervus terminalis in fishes may arise, at least in part, from the rostral end of the neural crest (Locy, ’05, and others). The mass of evidence, however, supports the thesis that in most animals tl1e nervus terminalis develops from elements derived from the olfactory placode. Cells from the forebrain may also contribute to the formation of the ganglion terminale. A migration of cells from the forebrain may well explain the presence of sympathetic ganglion cells. The receptive elements within the nerve are more likely derived from the olfactory placode. The bipolar and unipolar nerve cells are probably the sensory elements, while the multipolar neurons are more likely part of an autonomic component.


A satisfactory account of the nervus terminalis has not been given in any adult animal. The central course of the nerve has been described more completely in Necturus than in any other species (McKibben, ’11, and Herrick, ’33). Some of the terminalis fibers were thought to be sensory in Necturns, and these, after a partial decussation in the anterior commissure, end chiefly in the preoptic nucleus, the hypothalamus, and in the vicinity of the tuberculum posterius. Fibers were traced to the nucleus septi also. Further studies should be made in order to follow more completely the central course of this nerve. Dollken ( ’09) studied embryonic stages of man and of other animals and traced roots of the nervus terminalis to the gyrus fornicatus and to the septum pellucidum. The ventral place of entrance of the nervus terminalis is explained by the fact that the alar plate extends forward and ventralward in the region of the telencephalon (Ariéns Kappers, Huber and Crosby, ’36).


Embryonic material is not sufficient to give a complete picture of the peripheral distribution of the nervus terminalis. For instance, there are many glands in the nasal septum which have only begun to develop in the oldest material studied for this communication. Huber and Guild (’13) traced terminalis branches in young rabbits to the ducts of these septal glands.


The majority of workers have found that the ultimate nerve endings were not clearly defined.


It has been stated by a number of authors that the nervus terminalis is an independent nerve. The presence of this nerve in the porpoise, where the olfactory bulb is absent (Johnston, ’14), certainly would suggest that it is independent of the olfactory nerve. Johnston also reported that the nervus terminalis is larger in man than in many amphibians and fishes. While the central roots of the nervus terminalis are small in man, it is unlikely that this nerve is completely a vestigial structure. Brookover (’17) says that in the infant the peripheral part of the nerve is so large that it appears to be hypertrophied. It would seem that there must be some function for the many ganglion cells along its peripheral course. What this function may be is still a matter ofconjecture. Johnston (’13) states that the nervus terminalis in all vertebrates contains a receptive component which supplies ectodermal territory. There is evidence to support this claim. Huber and Guild (’13) and many others favor the interpreta— tion of an autonomic function, because of the anatomical character of the nerve. According to Larsell (’18) there are sensory and motor neurons in the nervus terminalis of mammals. Some of its sensory fibers were thought to end in the muscular walls of the anterior cerebral artery. Larsell considered the possibility of a vasomotor component. All ideas with regard to the function of the nervus terminalis are Within the realm of speculation. Concrete proof of function is still lacking. It is to be hoped that the newer physiological methods used in studying nervous activity may be employed to throw some light on this most interesting nerve.

Summary

The ganglion terminale is formed by the migration of cells and fibers from the medial border of the olfactory placode in the region of the anlage of the vomeronasal organ. These cells form groups along the medial border of the olfactory nerve.


The migration of these cells continues until one end of the ganglion terminale lies in contact with the ventromedial Wall of the forebrain. There is some evidence that cells migrate from the forebrain into the ganglion terminale. This migration may explain the origin of the sympathetic ganglion cells in the ganglion terminale. With further development and differential growth, the ganglion terminale becomes separated from the forebrain. The connection with the forebrain is retained by the fiber bundles which leave the caudal end of the ganglion and enter the forebrain in that region.


The fibers of the nervus terminalis in young embryos pass to the Ventral wall of the forebrain in a broad stream. In older embryos several nerve bundles may constitute the central roots of the nervus terminalis. These bundles course caudad from the ganglion terminale close along the medial border of the olfactory bulb and stalk. The roots of the nervus terminalis penetrate the ventromedial surface of the forebrain just caudal to the attachment of the olfactory bulb. The larger and more medially placed bundles course in the brain close to the surface for some distance. Some of these fibers reach the septal region of the brain.


The nervus terminalis is often differentially stained in pyridine silver preparations. This makes the course of the nervus terminalis distinct from other nerves in that region. From the rostral end of the ganglion terminale, a branch is given off which is distributed to the anterior region of the nasal septum. Some of its fibers are distributed to the epithelium of the septum. Bipolar ganglion cells migrate from this epithelium. Several nerve bundles leave the ventral border of the ganglion terminale and follow the branches of the vomeronasal nerve. Ganglion cells are scattered along the course of all the peripheral branches of the nervus terminalis. Cells migrate also from the vomeronasal organ.


The consensus is that the nervus terminalis is functional in mammals and that there are sensory and autonomic com ponents.

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