Paper - The development of the olfactory nerve in man (1941)
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The Development Of The Olfactory Nerve In Man
Anthony A. Pearson
Loyola University School of Medicine, Chicago, Illmois
Nine Figures (1941)
The olfactory nerve, the vomeronasal nerve, and the nervus terminalis are so intimately related in their development that it is difficult to describe one without some consideration of the other two. A description of any one of these nerves would naturally begin with the formation of the olfactory placode. The general plan of the development of the olfactory placode has been given in a number of the recent text—books of em— bryology. A description based on embryos stained with the general histological stains would be for the most part a useless repetition. The differentiation of the cells of the olfactory plaeode into the mature elements of the olfactory epithelium has not been described fully in human material. The lack of the early stages stained with adequate neurological methods forces the author to leave this part of the developmental history of the olfactory nerve until a future date. This communication deals primarily with the development of the olfactory nerve and its relation to the development of the olfactory bulb. A previous paper (Pearson, ’41) has discussed the development of the nervus terminalis.
This study is based on serial sections of human embryos prepared by various methods. The material used is listed below with certain necessary data. The letters B, E, and W indicate respectively the embryos that belong in the collections of Prof. G. W. Bartelmez of The University of Chicago, Prof. Martin Essenberg of Loyola University, and Prof. W.
F. Windle of Northwestern University. The others listed are in the author’s collection. The methods of preparation have been given in a previous paper (Pea.rson, ’38). The author acknowledges his indebtedness to Professors Bartelmez, Essenberg, and Windle.
CROWN-RULIP PROBABLE 1-2 M’él&‘€§o. Mggggggwgs gvgggg 1=‘£.‘§§§§‘».’.ii»?;.‘"N E 206 9% 5} Hematoxylin B 808 14 6 Copper protargol (Bodian) W 698 16 6 Pyridine silver 48 17 7 Copper protargol 16 17 7 Pyridine silver 31 22 7 -} Copper protargol B 1194 25 81} Pyridine silver 29 29 9 Copper protargol 34 36 9§ Copper protargol 30 38 10 Copper protargol 21 45 1]. Copper protargol 22 46 11 Copper protargol 45 78 13 Copper protargol
The Olfactory Nerve
It is diﬂicult to determine at just what period neuroblasts begin to develop in the olfactory placode of human embryos. Bipolar cells which resemble olfactory nerve cells were observed in the olfactory placode of a 9.5 mm. human embryo. Although this embryo was not stained with a neurological stain, a few nerve ﬁbers could be traced from the placode into the mesoderm. These ﬁbers were ﬁne and lightly stained; consequently they could not be followed for any appreciable distance.
Bedford (’04) observed cells in pig embryos which had migrated from the nasal epithelium into the mesoderm. Many of these cells were arranged in cords which converged near the brain and united to form a cellular mass. At ﬁrst this mass had no connection with the brain. Fibers are said to precede the migration of cells from the olfactory placodein rabbit embryos (Van Campenhout, ’36). Whether this is the case in human material is difficult to determine. Evidences of a migration of cells from the olfactory epithelium can be observed in young human embryos. With the migration of cells and the growth of olfactory nerve ﬁbers toward the brain, a bundle is formed which stretches obliquely upward from the olfactory epithelium to the ventral wall of the telencephalon (ﬁg. 1). This bundle of ﬁbers constitutes the
bulb. olf., bulbus olfactorius lam. fib. N. o1f., lamina ﬂbrarum nervi bulb. olf. acc., bulbus olfactorius acces- olfactorii sorius N. olf., nervus olfactorius
c., cartilage N. term., nervus terminalis
ﬁla o1f., ﬁla olfactoria olf. epi., olfactory epithelium
gang. term., ganglion terminale v., or vent., ventricle
Fig. 1 A sagittal section ‘through the forebrain and the olfactory nerve of a 17 mm. human embryo (no. 48). Copper pi-otargol preparation (section 7-1-3). X 34.
embryonic olfactory nerve. This nerve is well shown in a 14 mm. human embryo (see fig. 1, Pearson, ’41). Due to the fact that the olfactory nerve passes "obliquely upwards toward the brain, only a small part of the nerve will be seen in any one transverse section. The olfactory nerve ﬁbers arise from cells in the epithelium which forms the dorsal boundary of the nasal fossa in the region lateral to the anlage of the vomeronasal organ. Along the medial side of the olfactory nerve are elements which form the ganglion terminale and the vomeronasal nerve. His (1889) considered this mass to be an integral part of the olfactory nerve and referred to it as the “olfactory ganglion”. Simonetta (’32) recognized two parts in the so-called “olfactory ganglion” of human embryos: a medial part (the ganglion terminale) which contained cells resembling neuroblasts, and a lateral part (the olfactory portion) containing small cells.
The olfactory nerve stains poorly in these young embryos and therefore it is not easy to determine at just what period the nerve ﬁbers begin to grow into the brain. The available material would indicate that olfactory nerve ﬁbers have begun to enter the brain by the sixth week of human development. Several bundles of these ﬁbers are shown entering the forebrain of a 16 mm. human embryo (ﬁg. 2). Some of the more medially placed ﬁbers may belong to the nervus terminalis. It was not possible to distinguish the two nerves with certainty in this embryo. These ﬁber bundles break up among the more superﬁcially placed cells after entering the brain. Within the brain some of the ﬁbers turn mediad and others turn laterad.
Fig. 2 A transverse section of the fcrebrain at the level of the entrance of the ﬁbers of the olfactory nerve. Some of the more medially placed ﬁbers may be part of the nervus terminalis (a 16 mm. human embryo no. W 698). Pyridine silver preparation (section 15—-1-2). X 30.
It has been pointed out that the course of the olfactory nerve is obliquely upward and toward the rostral end of the brain. For this reason the nerve can be seen best in the sagittal series. In a 17 mm. human embryo (no. 48) cords of cells and ﬁbers converge to form the olfactory nerve (ﬁg. 1). While the nerve extends up to the ventral wall of the forbrain in this embryo, it was not possible to trace ﬁbers into the brain itself. This was thought to be due to the light stain of the nerve ﬁbers. No evidence was observed which would indicate that elements from the brain itself take part in the formation of the olfactory nerve.
At the time of the formation of the anlage of the olfactory nerve, there is no indication of an olfactory bulb. Bedford (’04) made the same observation of the olfactory lobe in pigs. There is still no indication of a bulb even when the olfactory nerve ﬁrst becomes attached to the brain (ﬁgs. 1 and 2). Soon after the olfactory nerve ﬁbers begin to grow into the brain, the olfactory bulb begins to show signs of development. A 17 mm. human embryo (no. 16) shows a slight bulge in the region Where the olfactory nerve is attached to the brain. A slight depression on the inside of the brain corresponds in position to the bulge on the outside (ﬁg. 3). This embryo was ﬁxed in ammoniated alcohol and thus shows much more shrinkage than no. 48 (ﬁg. 1) which was ﬁxed in a mixture of formalin, acetic acid, and alcohol.
Fig. 3 A sagittal section through the forebrain of a 17 mm. human embryo (no. 16). A slight protrusion of the forebrain in the region of the attachment of the olfactory nerve indicates the anlage of the olfactory bulb. The olfactory region appears to be slightly further developed than in ﬁgure 1. Pyridine silver preparation (section 7-3-2). X 34.
With further development there is an increase in the size of the olfactory nerve. This is well shown in a 22 mm. human embryo (no. 31, fig. 4). The increase in the size of the olfactory nerve is due to the additional growth of ﬁbers from the olfactory epithelium. One end of this mass of ﬁbers and sheath cells, which is here designated the olfactory nerve, lies in contact with the developing’ olfactory bulb. The 01factory bulb is now a distinct protrusion of the wall of the telencephalon into which the ventricle of the brain continues. The bulb is directed downward and slightly backward. The layers of the wall of the forebrain continue into the bulb uninterrupted. At this period the wall of the tclencephalon is formed mainly by the mantle and ependymal layers. The external limiting membrane of the brain is not clear in the region of the junction of the bulb and the olfactory nerve, and the boundary is not sharply deﬁned. An occasional small blood vessel or capillary which runs between the two may indicate a boundary. The proximal end of the olfactory nerve covers the olfactory bulb like a cap.
Fig. 4 The relation of the developing olfactory bulb and the olfactory nerve is shown in a sagittal section of a 22 mm. human embryo (no. 31). Copper pi-otargol preparation (section 13-1-3). X 34.
In young embryos (e.g., no. 31, 22 mm.) the ganglion of the nervus terminalis lies along the caudomedial aspect of the olfactory nerve. The attachment of the nervus terminalis to the brain is just caudal to the attachment of the olfactory nerve. A small blood vessel often separates the two (ﬁg. 4). Certain sections of this sagittal series reveal the close relation of these two nerves (ﬁg. 5). An irregular boundary can be seen between them. It is diﬁicult to say, however, whether there is a mixing of the elements of the two nerves in such places. The ganglion terminale contains a large number of ganglion cells which stand out in contrast to the small cells among the ﬁbers of the olfactory nerve. The small cells among the ﬁbers of the olfactory nerve are thought to develop into sheath cells. For this reason the olfactory nerve in these young stages is not called a ganglion. It is not possible to rule out the presence of scattered ‘ganglion cells which may have wandered in from the ganglion terminale. Figures 2, 4, 6, and 8 in a previous paper (Pearson, ’41) further illustrate the relation of the olfactory nerve to the nervus terminalis.
Fig. 5 A sagittal section slightly medial to the plane of ﬁgure 4. Note the close relation of the olfactory nerve and the ganglion terminale. Copper protargol preparation (human embryo no. 31, section 13-2-3). x 34.
The protrusion of the forebrain which gives rise to the olfactory bulb continues to enlarge for a period. A sagittal section through the brain of a 29 mm. human embryo (no. 29) reveals a slight constriction at the base of the developing bulb. This constriction indicates the future boundary between the bulb proper and the rest of the brain (ﬁg. 6). The bulb now points more directly downward and medialward. The cerebral cortical layers are in the process of formation in embryos of this age, but they do not extend into the olfactory bulb. These layers of cortical cells fuse with the ependymal layer as they approach the bulb region. The wall of the growing olfactory bulb is thinnest at its distal end. Here the wall is formed principally by the ependymal layer of cells.
Fig. 6 A sagittal section through the developing olfactory bulb of a 29 mm. human embryo (no. 29). Copper protargol preparation (sections 11-2-1 and 2). X 24.
The mass of ﬁbers and cells which constituted the olfactory nerve in younger embryos is in the process of being incorporated as a part of the olfactory bulb. The embryonic olfactory nerve is now seen as a loose plexus of ﬁbers and cells (sheath) which forms a layer partially covering the surface of the olfactory bulb. This layer becomes known as the layer of olfactory nerve ﬁbers and it is usually listed as one of the layers of the olfactory bulb. The nerve ﬁbers arising in the olfactory epithelium have increased in number and are grouped in small bundles. These are known as the ﬁla olfactoria and they pass into the layer of olfactory nerve ﬁbers of the bulb.
The olfactory bulb in a 36 mm. human embryo (no. 34) is much larger than in the preceding 29 mm. embryo. While the bulb is still directed downward, it is now directed slightly forward and medialward. With the additional growth of olfactory nerve ﬁbers from the olfactory epithelium, the layer of olfactory nerve ﬁbers of the bulb has increased.
The olfactory bulbs are well shown in the cross sections of a 38 mm. human embryo (no. 30, see ﬁg. 9, Pearson, ’41).
Fig. 7 A sagittal section through the olfactory bulb region of a 11 weeks human fetus (no. 21). Copper protargol preparation (section 40-2-2). X 18.
The layer of olfactory nerve ﬁbers has spread out more and it now covers the rostral end and the Ventromedial surface of the olfactory bulb. The ﬁla olfactoria converge as they approach the rostral end of the olfactory bulb and enter the more medial aspect of the ﬁber layer covering the end of the bulb.
As the olfactory bulb continues to grow, it is gradually directed forward (ﬁg. 7). This rotation of the bulb was noted by Von Kolliker (1882) and Humphrey (’40). The developing layers of cortical cells are clearly shown in human embryos about 11 weeks of age (nos. 21 and 22). The layers of cortical cells now extend into the region of the junction of the olfactory bulb with the rest of the telencephalon. They do not continue into the olfactory bulb as deﬁnite layers. In human embryos approaching the age of 2 months, the layer of olfactory nerve ﬁbers more nearly surrounds the olfactory bulb, particularly on the medial side. While there is no sharp line indicating a boundary between the layer of olfactory nerve ﬁbers and the rest of the olfactory bulb, a boundary can be seen. This boundary is due to the difference in the histological character of this layer of ﬁbers from the rest of the olfactory bulb. The author is not certain whether there is an external limiting membrane separating the layer of olfactory nerve ﬁbers from the bulb proper as is the case in the Arnphibia (Herrick, ’31). The nuclei in the cells of the layer of olfactory nerve ﬁbers are smaller, more darkly stained, and more closely placed than in the adjoining region of the bulb. At intervals, ﬁber bundles leave this layer of ﬁbers and pass more deeply into the bulb. The nuclei of the nerve cells deep to the layer of ﬁbers have begun to enlarge. These are probably the nuclei of mitral cells which have begun to differentiate. The ventricle continues farther forward into the olfactory bulb than is shown in ﬁgure 7. The ﬁla olfactoria have continued to increase in size and in number, and converge toward the olfactory bulb in large and in small bundles. These bundles pass into the part of the layer of olfactory nerve ﬁbers which covers the rostral end and the ventromedial side of the olfactory bulb. The ﬁbers from approximately the rostral half of the olfactory epithelium in embryos of 11 weeks tend to enter the more rostral half of the olfactory bulb. These as a rule are grouped in small bundles which, on approaching the bulb, branch and anastomose. The ﬁla olfactoria which come from the caudal half of the olfactory epithelium may be roughly classed into two groups: those from the lateral and those from the medial walls of the olfactory sac. The bundles from the lateral wall enter the ventral side of the olfactory bulb. The ﬁla olfactoria from the medial wall converge into large bundles which may be followed into the ventromedial side of the bulb.
After the bulb turns forward it begins to grow more in length than in thickness. This is well shown in the sagittal sections of a 78 mm. human embryo (no. 45). In order to present a more complete picture, the essential features of several sections have been incorporated into ﬁgure 8. This makes it possible to show that the ventricle of the brain still continues out into the olfactory bulb. The ﬁla olfactoria enter the more medial aspect of the bulb and would not ordinarily appear in this ﬁgure. With the formation of the cribriform plate the ﬁla olfactoria are collected into fewer but larger bundles. Below the cribriform plate the ﬁla olfactoria are thought not to branch and anastomose. Many of the early investigators considered that the bundles of the olfactory nerve ﬁbers had a plexiform arrangement. Read (’08) was one of the ﬁrst to point out the fallacy of this conception. The large size of the ﬁla olfactoria and the increased thickness of the layer of olfactory nerve ﬁbers of the bulb are evidences of an increase in the number of nerve ﬁbers which have grown in from the olfactory epithelium. The layer of olfactory nerve ﬁbers covers more of the surface of the olfactory bulb as the latter continues to grow in size. Many small bundles of ﬁbers leave the layer of olfactory nerve ﬁbers and sink deeply into the bulb. At the fetal age of 3 months secondary olfactory connections are in the process of being established. These connections, however, are beyond the scope of this paper. The layers of cortical cells are further developed in this fetus. These layers of cells continue into the bulb for only a short distance where they abruptly blend with the gray of the bulb.
Fig. 8 A composite drawing made from several sagittal sections through the olfactory bulb region of a human fetus of about 13 weeks (no. 45). Copper protargol preparations (slides 78, 81, 84, and 85). X 13.
It is quite evident that sheath cells are derived from cells migrating from the olfactory placode. This migration begins early in the development of the olfactory nerve and probably continues over a considerable period of its development. Clusters and cords of cells are quite prominent along the course of certain of the ﬁla olfactoria in fetuses of 11 weeks. Those migratory cells demand further study and a more complete discussion will be given in a later paper. The origin of sheath cells from the olfactory placode has been observed by a number of authors (Disse, 1897, Van Campenhout, ’36, and others).
The Accessory Olfagtory Bulb
There is an area along the dorsomedial side of the developing olfactory bulb, which is thought to correspond to the accessory olfactory bulb in lower forms (McCotter, ’12). Recently Humphrey (’40) has described this formation in human fetuses. This area is located dorsal and caudal to the layer of olfactory nerve ﬁbers, and rostral to the place where the largest root of the nervus terminalis enters the brain (ﬁgs. 7 and 8, see also ﬁg. 9, Pearson, ’41). It was not possible to demonstrate a large root of the vomeronasal nerve to the accessory olfactory bulb, such as McCotter (’12) has described for the rabbit and the opossum. Instead, a number of smaller bundles leave the lateral aspect of the vomeronasal and nervus terminalis complex and enter the medial side of the olfactory bulb just in front of and along the lower border of the accessory olfactory bulb. The arrangement of the roots may be subject to variation, for it was not possible to trace the central connections of this nerve as distinct roots in all of the human embryos studied. The lack of‘ a conspicuous root to the accessory olfactory bulb is not altogether surprising, for the comparative studies of McCotter (’12) indicate that the size of the accessory olfactory bulb varies directly with the size of the vomeronasal organ, from which it receives ﬁbers through the vomeronasal nerve. The vomeronasal organ is generally considered to be rudimentary in man as it usually atrophies in later development. It may completely degenerate during fetal life, but it has been found in adults. The epithelium of the vomeronasal (Jacobson’s) organ in the rabbit has been shown to contain nerve cells similar to olfactory nerve cells (Von Lenhossék, 1892). This is true at a certain period of human development. The organ is like a pocket of olfactory epithelium in the wall of the nasal septum. It is thought to be a highly specialized part of the olfactory apparatus and it is probably functional in such forms as the rabbit. As the bulb grows in length the accessory olfactory bulb tends to keep its original position near the attachment of the olfactory bulb to the brain. It is still a landmark in a 78 mm. human fetus (ﬁg. 8). The accessory olfactory bulb does not appear to have grown appreciably in size, and by comparison with the rest of the olfactory bulb, it is smaller. The accessory olfactory bulb is thought to be lacking in the adult human brain (Humphrey and Crosby, ’38). An area denuded of olfactory formation was found in the region where the accessory olfactory bulb is located in certain lower forms. The peripheral course of the vomeronasal nerve is intimately tied in with that of the nervus terminalis (Pearson, ’41, see ﬁgs. 10 and 13).
Ehrlich (1886) used methylene blue to demonstrate that the ﬁla olfactoria are the processes of bipolar cells located in the olfactory epithelium. Other workers (Ramon y Cajal, 1890, and Van Gehuchten, 1890) conﬁrmed his observations by the use of the Golgi method, and thus the true character of the ﬁla olfactoria became established. Many of the earlier investigators failed to understandthe structure of this nerve and consequently held erroneous ideas concerning its development. Some observers (Balfour, 1877) believed the olfactory nerve to be an outgrowth from the brain. Marshall (1.878) concluded that the olfactory nerve in the chick develops from the neural crest. Others (Beard, 1885, and Chiarugi, 1891) claimed that the anlage of the olfactory nerve arises from the brain and the olfactory epithelium. Cameron and Milligan (’14) described the embryonic olfactory nerve as a nucleated protoplasmic bridge which brought the olfactory end-organ into direct structural continuity with the forebrain. To this nucleated tra-ct of cytoplasm they applied the term, “olfactory syncytium”. 1
His (1889) was one of the first to point out that the olfactory nerve grows in from the periphery. He described the formation of an “olfactory ganglion” through the migration of neuroblasts toward the brain. The upper end of the ganglion was thought to join the anterior olfactory lobe, while the lower or peripheral end was connected with the olfactory placode. According to Bianchi (’31 a) the term, “olfactory ganglion”, is not proper because the elements which constitute the ganglion are part of the nervus terminalis and because the elements which are in relation to the olfactory nerve form the sheaths of the ﬁbers of the olfactory nerve. At the time His studied the development of the olfactory region, the nervus terminalis had not been identiﬁed in mam— mals. For this reason it is not surprising that he included the ganglion terminale as a part of the olfactory nerve.
The work of His (1889) indicates that the olfactory lobes appear at the beginning of the second month of human development as the result of a differentiation of a part of the walls of the cerebral hemispheres. Anterior and posterior olfactory lobes were said to develop. The anterior olfactory lobe developed into the olfactory bulb and tract. Olfactory nerve ﬁbers were thought to grow from the “olfactory ganglion” to the anterior olfactory lobe. Bianchi (’31 b) observed a cord of cells extending between the olfa-ctory fossa and the telencephalon before the appearance of the olfactory bulb. In the human material studied for this communication, the olfactory bulb shows no signs of development until some time after the initial attachment of the olfactory nerves to the cerebral hemispheres. This is well illustrated in ﬁgures 1, 2, 3, and 9.
Fig. 9 A series of drawings illustrating the development of the human olfactory bulb as revealed in sagittal sections. The following stages are shown: a. at 17 mm.; b, at 17 mm. (slightly older than a); c, 22 mm.; <1, 25 mm.; c, 29 mm.; f, 45 mm.; g, 78 mm. Approximately >( 7.
The development of the olfactory bulb reminds one of Kipling’s story, “The elephant’s child”. The suggestion is not being made that the embryonic olfactory nerve actually pulls part of the brain" wall out into a prolongation which becomes the olfactory bulb. However, the olfactory nerve probably does exert a great inﬂuence on the development of the olfactory bulb. Detwiler (’36) suggests that the relation between the olfactorynerve and the brain is a reciprocal one. The actively proliferating cells of the developing cerebral hemisphere attract the growing olfactory nerve ﬁbers and direct their entrance into the brain (Coghill, ’24, and Burr, ’32). The entrance of the nerve into the wall of the brain stimulates the cells in that region to increased mitotic activity (Burr, ’30). The resulting hyperplasia undoubtedly plays a role in the formation of the olfactory bulb, and its degree of development is probably in proportion to the number of olfactory nerve ﬁbers entering the brain. The hyperplasia is thought to be the result of a stimulus associated with the ingrowing axons rather than of the functional activity of the sense organ (Burr, ’30).
The relation of the olfactory ne-rve to the developing olfactory bulb in a 22 mm. human embryo *(ﬁg. 4) resembles that of amphibia. Herrick (’31) described the olfactory nerve in N ecturus as spreading out to form an “implantation cone” which covers the rosterolateral aspect of the olfactory bulb. His (1889) recognized that the central end of the anlage of the olfactory nerve persists as a covering for the olfactory bulb.
Humphrey (’40) has shown that in later development (i.e., a fetus of 18.5 weeks) the layer of olfactory nerve ﬁbers surrounds the olfactory bulb more completely, particularly at the frontal tip. This layer of ﬁbers does not extend as far caudalward on the lateral surface as it does on the ventramedial surface of the olfactory bulb. Humphrey has also pointed out that cells from the ependyma begin to grow into the olfactory ventricle at about the fourteenth week of menstrual age and that by the nineteenth week the olfactory ventricle has been obliterated.
The anlage of the olfactory nerve is formed by the growth of ﬁbers and the migration of cells toward the brain. These form a bundle which stretches obliquely upward toward the ventral wall of the telencephalon. This bundle of ﬁbers constitutes the embryonic olfactory nerve. The ﬁbers of the olfactory nerve arise from cells located in the epithelium which forms the dorsal boundary of the nasal fossa in the region lateral to the vomeronasal organ. The olfactory nerve increases in size due to the additional growth of ﬁbers from the olfactory epithelium. V 1 .
There is no indication of an olfactory bulb at the time of the initial attachment of the olfactory nerve to the forebrain. After the olfactory nerve ﬁbers begin to grow into the brain, a slight protrusion develops on the -wall of the brain in the region where the olfactory nerve is attached. This protrusion indicates the beginning of the development of the olfactory bulb. The olfactory__bulb develops as an evagination of the wall of the forebrain directed downward, backward and medialward. As development continues, it is gradually directed forward.
The proximal end of the olfactory nerve covers the developing olfactory bulb like a cap. As the olfactory bulb enlarges, the embryonic olfactory nerve spreads out into a layer of ﬁbers which partially covers the surface of the bulb. This layer, becomes an integral part of the olfactory bulb and is known as the layer of olfactory nerve ﬁbers. The number of olfactory nerve ﬁbers arising in the olfactory epithelium gradually increases and the ﬁbers become grouped into small bundles. These are known as the ﬁla olfactoria. and they pass without interruption into the layer of ﬁbers which covers the bulb. With the formation of the cribriform plate, the ﬁla olfactoria are gathered into fewer but larger bundles. The olfactory nerve ﬁbers are not to be confused with the nervus ‘terminalis which is a distinct and separate nerve. The term “olfactory ganglion” as used by His (1889) is discarded because it is thought to include the ganglion of the nervus terminalis.
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Cite this page: Hill, M.A. (2020, October 31) Embryology Paper - The development of the olfactory nerve in man (1941). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_development_of_the_olfactory_nerve_in_man_(1941)
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