Paper - The trochlear nerve in human fetuses

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Pearson AA. The trochlear nerve in human fetuses. (1943) J. Comp. Neurol. : 29-43.

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This historic 1943 paper by Pearson described development of the fetal human trochlear nerve CN IV.


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 development of the nervus terminali in man. (1941) J. Comp. Neurol. 75: 39-66.

Pearson AA. The oculomotor nucleus in the human fetus. (1944) J. Comp. Neurol. 47-.

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Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

The Trochlear Nerve in Human Fetuses

Anthony A. Pearson


Loyola University School of Medicine, Chicago, Illinois

Ten Figures (1943)

Introduction

The early development of the trochlear nerve in mammalian embryos has been described by Windle (’32 a, ’32 b), Zahajszky ( ’40), and others. The discussion will be limited to the later development of the trochlear nerve and its relation to the trigeminal nerve.‘ This study is based on serial sections of human embryos and fetuses stained with various silver methods. The whole heads of the smaller fetuses and em— bryos were sectioned and studied; however, only the brains of the larger fetuses were prepared. Most of the material used in this study has been listed in previous papers (Pearson, ’41 a, ’41 b) and only necessary data will be given here.

Nucleus Of Origin

The nucleus of the trochlear nerve is easily recognized in older human embryos and fetuses as a large mass of multipolar neurons located just caudal to the nucleus of the oculo— motor nerve. There is no wide interval between the nuclei of the third and fourth cranial nerves. A distinct thinning out of the cells of the motor column, however, indicates a boundary between the nuclei of these two nerves. The trochlear nucleus is in line with the lateral groups of cells of the oculomotor nucleus. It is located i11 its characteristic position, dorsal to and partly imbedded in the medial longitudinal fasciculus.


The nucleus of the trochlear nerve is formed by one main mass of cells and sometimes by an additional smaller mass of cells which lies farther caudad (figs. 1, 2, 3). The caudal group of cells may be bilateral or unilateral. VVhen it is unilateral, it may occur on either the right _or the left side.


This subdivision of the trochlear nucleus into a larger cephalic portion and a smaller caudal portion has been observed by several investigators (Sabin, ’O1; Tsuchida, ’06; van Valkenburg, ’12; and Sano, ’41). Tsuchida reported a subdivision in the trochlear nucleus in some 20 to 30% of the brainstems studied, this differentiation occurring in most of the specimens on only one side. In the material studied‘ by the author the percentages were somewhat higher. The caudal division of the trochlear nucleus occurred nearly as often on both sides as on only one side. When the caudal division was present on one side only, it was found to occur about as frequently on the right side as on the left side.


ABBREVIATIONS

aq.cer., or cer.aq., aquaeductus cerebri

cer., cerebellum

c.mes.V., cells of the mesencephalic root /of V

dcc.N.IV, decussation of the trochlear nerve

f.1.m., fasciculus longitudinalis medialis

4th vent., fourth ventricle

gang.N.V, ganglion semilunare

med.ob1., medulla oblongata

me.root V, mesencephalic root of the trigeminal nerve

mes.V et nu., mesencephalic root of V and nucleus

N.III, nervus oculomotorius

N .IV, ncrvus trochlearis

N.V, nervus trigeminus

nu.IV, nucleus nervi trochlearis

nu.IV p.caud., nucleus trochlearis (pars caudali)

V., or vent., ventriculus

X, 3. group of cells in the path of the trochlear nerve


Fig. 1 A agittal section through the brainstem of a 29-mm. human fetus (no. 29). Note the rostral and caudal divisions of the trochlear nucleus. Copper protargol preparation (section 16-1-2). X 12.


Fig. 2 A transverse section through the mesencephalon of a 5-month-old fetus (no. 64) at the level of the main nucleus of the trochlear nerve. In the left nucleus of the IV nerve there are two cells of the mesencephalic V type. Pyridine silver preparation (section 29-3-4). X 24.


In one human fetus of about 5 months of age (no. 63) the trochlear nucleus on each side was a single mass of cells. In another fetus (no. 64) of about the same age, there was a caudal division of the trochlear nucleus on each side (fig. 3). This caudal division was a small group of darkly staining Inultipolar neurons. It was located about 1 mm. caudal to the


Fig. 3 A transverse section through the mesencephalon of a 5-month-old fetus (no. 64) at the level of the caudal division of the trochlear nucleus. Pyridine silver preparation (section 24-3-3). X 24.

main nucleus and was approximately 0.2 mm. in length. This caudal nucleus of the trochlear nerve was slightly smaller on the right side than on the left. There are about sixty cells in the caudal nucleus on the right side and about eighty-three cells on the left side. This is only an approximation, as the cells were closely packed and it was difficult to make an exact count. In the fetus which possessed only the main nucleus of the trochlear nerve it is interesting to note that this main nucleus measured slightly more than 1 mm. in length and was quite symmetrical. In the other fetus of this same age, tl1e main nucleus measured less than 1 mm. in length. On the right side, the main nucleus was about 0.9 mm. in length and the caudal division contained about sixty cells. The main nucleus of the trochlear nerve on the left side measured about 0.6 mm. and the caudal division contained about eighty—three cells. The cross sectional area of the main nuclei of the trochlear nerve in both fetuses appeared to be approximately equal. These two fetuses are thought to be fair examples of the cellular arrangement of the trochlear nerve nuclei. This suggests that the size of the main nucleus is in inverse proportion to the size of the caudal division. There is no indication that the fiber connections of the caudal division are any different from those of the main nucleus of the trochlear nerve nor is there any apparent physiological significance to the separation of the cells of the trochlear nerve into groups.

A few cells of the mesencephalic V type were observed in the main nucleus of the trochlear nerve (fig. 2, left). These cells are easily distinguished from the usual multipolar neurons of the trochlear nucleus by their shape and size. Weinbe1'g' (’28) has made a similar observation.

In certain embryos, scattered cells have been observed along the course of the trochlear nerve central to its" decussation (fig. 4). These cells are thought to resemble neuroblasts, although their exact character is diflicult to determine. Occasionally, such cells form a distinct cluster. In one 3-month-old human fetus, such a group was found in the central course of the trochlear nerve on each side (fig. 5). This group is located dorsolateral to the medial longitudinal fasciculus and at a plane slightly caudal to the level of the trochlear nuclei. Some of the cells appear to be bipolar, although their exact shapes are not distinct. Sabin (’01) has also reported the presence of groups of cells along the root fibers of the trochlear nerve.


Fig. 4 A sagittal section through the brainstem of a 17-mm. human embryo (no. 16). Scattered cells are shown along the course of the trochlear nerve. Pyridine silver preparation (8—3~2). X 75.

cm. car,


Fig. 5 A transverse section through the mesencephalon of 9. 63-mm. human fetus (no. 57). A small cluster of cells is hown in the path of the IV nerve. Copper protargol preparation (section 48—2—3). X 14.


The Course of the Nerve

Fibers of the trochlear nerve are collected into several small bundles along the dorsolateral border of the trochlear nucleus toward its caudal end. When a caudal division of the trochlear nucleus is present an additional bundle of fibers arises here. This bundle soon joins the larger bundles of the trochlear nerve. The fibers of the trochlear nerve follow an oblique course through the periphery of the central gray which surrounds the cerebral aqueduct. At first the fibers pass dorsolaterad. On reaching the lateral part of the central gray, the course of the trochlear nerve fibers is directed caudad and dorsad. The caudal course of the nerve is attributed in part to the shifting forward of the cells of origin during development (Ariens Kappers, Huber, and Crosby, ’36). The fibers of the trochlear nerve runalmost parallel to the mesencephalic root of the trigeminal nerve for a short distance. As the fibers of the trochlear nerve approach the anterior medullary velum, they begin to turn toward the midline. Here they lie almost perpendicular to the fibers of the mesencephalic root of the trigeminal nerve. As the midline is approached, the fibers of the trochlear nerve can then be traced into the ventral part of the decussation of that nerve. After they pass to the other side, the fibers of the trochlear nerve emerge from the decussation and make their exit from the dorsolateral surface of the brainstem. No trochlear fibers were observed which failed to decussa.te as van Gehuchten (’03) noted in the rat and rabbit. ' The course of the trochlear nerve within the brain lies deep, but close to the mesencephalic root of the trigeminal nerve and the nucleus of that root. It has been suggested by several authors that there are connectionsxbetween the mesencephalic root of the trigeminal nerve and the trochlear nerve (Freeman, ’27, Weinberg, ’28 and others). Such a connection has been difficult to demonstrate or rule out. There are cells of the mesencephalic V type, however, which are thought to be definitely related to the trochlear nerve. Cells of this type occasionally occur -in the trochlear nucleus (fig. 2), as already mentioned. There are cells of the mesencephalic V type in the region lateral to the anterior medullary velum. Some of these cells appear to be connected with the trochlcar nerve. An occasional cell may be found directly in the course of this nerve (fig. 7). These cells may appear singly or in clusters. Occasionally, a process of one of these cells may be followed directly among the fibers of the trochlear nerve (fig. 8). A few scattered cells of the mesencephalic V type may be found in the anterior medullary Velum. An example of one of these cells is shown in figure 9. A bipolar cell is shown in the anterior medullary velum lying; ventral to the fibers of the trochlear nerve. A process from either end of the cell extends out among the fibers of the trochlear nerve. A similar cell was described by Golgi (1893). V-*'indle (’32 a) described a cell which sent one branch into the trochlear nerve and another branch into the mesencephalic tract of a cat.


Fig. 6 A diagram made from several sagittal sections of the brainstem of 2: 25-mm. human embryo (no. B. 1194). Pyridine silver preparation (13-20).


Fig. 7 A section through the trochlear nerve within the rnesencephalon. Note the nerve cell in the path of the nerve. From a 5»month—old human fetus (no. 64). Pyridine silver preparation (19—3—4).


Fig. 8 A transverse section through the mesencephalon of a 5-m.onth~old fetus (no. 64) at the level of tl1e anterior medullary velum. Note the close relation of the IV nerve to the meseneephalie root of the V nerve and its nucleus. Pyridine silver preparation (section 21-3-3). X 94.


Fig. 9 A photomicrograph of a nerve cell in the anterior medullary velum of a. 5—month—old human fetus (no. 63). The processes of the nerve cell extend dorsally among the fibers of the troehlear nerve. Pyridine silver preparation (193—4). X 450.


Peripheral to the decussation in the anterior medullary veluin, the fibers of the trochlear nerve leave the dorsolateral surface of the brainstem grouped in one or two small bundles. After leaving the brain, these fibers collect into a single small trunk, which can be traced ventrad close along the surface of the brainstem. Before reaching the orbit the fibers of the trochlear nerve pierce the dura mater and pass forward between the layers of the tentorium cerebelli.

As the trochlear nerve passes forward to enter the orbit it is joined by a small bundle of fibers from the ophthalmic division of the trigeminal nerve. This branch of the trigeminal nerve leaves the ophthalmic division just peripheral to the semilunar ganglion. It joins the trochlear nerve (figr. 10) and may be followed back toward the brain. Part of these fibers are thought to be distributed to the dura mater along the course of the trochlear nerve. A few of them can be followed between the layers of the dura mater into the 1'0/gion of the transverse sinus.

Just peripheral to the place where the above anastomotic branch joins the trochlear nerve, a short part of the course of the trochlear nerve lies in intimate relationship with the ophthalmic nerve. The fibers of the two nerves lie so close together that it is extremely difficult to determine in serial sections whether there is an exchange of fibers between them. After crossing the ophthalmic nerve, the trochlear nerve may be traced forward into the superior oblique muscle. The part of the trochlear nerve peripheral to the place where it crosses the ophthalmic nerve is larger than the part of the nerve at its exit from the brain. This difference in size is sufficient to lead one to conclude that the trigeminal nerve contributes fibers to the distal part of the trochlear nerve.


The lacrimal nerve occasionally receives ‘a small branch from the trochlear nerve. This contribution to the lacrimal nerve is probably composed of fibers which are derived from the ophthalmic nerve and which simply accompany the trochlear nerve for a short distance. It has been reported that the trochlear nerve occasionally sends a branch to the orbicularis oculi muscle (Piersol, ’30).‘ This branch, however, was not observed in any of the material studied by the author. In addition to the other communicating branches already mentioned, there are small filaments from the cavernous plexus of nerves Which join the trochlear nerve.

Fig. 10 A diagram drawn from the sagittal sections of the brainstem of a 36-mm. human fetus (no. 34) showing a portion of the course of the trochlear nerve. Copper protargol preparation.

Discussion

The investigations of several authors (Huber, ’00; Tozer and Sherrington, ’10, and others) have shown that there are sensory endings in the extrinsic muscles of the eye and that these endings degenerate after cutting the third and fourth cranial nerves (Tozer and Sherrington, ’10, and Tarkhan, ’34) . It has been more difficult to demonstrate clearly the location of the cell bodies of the sensory neurons involved.


The anatomical evidence submitted here would indicate that the proprioceptive neurons for the superior oblique muscle are of the mesencephalic V type. They are thought to be located in the brainstem close to the level of the trochlear nerve. The details of the connections of these neurons have been discussed, and they are in general agreement with the position taken by Weiriberg (’28) and Tar-khan (’34) on this question. The experimental work of Freeman (’27), Tarkhan_ (’34), and others strongly suggests that there are proprioceptive fibers in the fourth cranial nerve. The existence of proprioceptive neurons is indicated, after the removal of the orbital contents, by changes in the cells of the mesencephalic nucleus at the level of the trochlear nerve (Freeman, ’27). Corbin (’40) states that such fibers from the mesencephalic nucleus do not join the trochlear nerve extracranially from branches of the trigeminal nerve. Corbin and Harrison (’40 and ’42) found that no action potentials were elicited from the mesencephalic root of V as a result of stretching the extrinsic muscles of the eye. It was possible, however, to obtain action potentials from the oculomotor nucleus and the intramedullary portion of the oculomotor nerve. Corbin (’40) pointed out that if cells of the mesencephalic nucleus do contribute fibers to the trochlear nerve, this contribution must come from cells located between the levels of the trochlear nucleus and the decussation of that nerve. It seems quite likely that the majority of the cells in question may occupy this position. Tozer (’12), however, found no change in the meseneephalic nucleus after cutting the third and fourth cranial nerves. VVe thus have experimental evidence for and against the theory that eertainlcells of the mesencephalic nucleus contribute fibers to the trochlear nerve. It should be remembered that the results gained from the chromatolysis of cells and the Marchi method are not always reliable and that conclusions should be made with care. The more recent Work of Corbin and Oliver (’42) further indicates that the extrinsic ocular muscles are not innervated by the mesencephalic root of the fifth nerve. These authors are of the opinion that the cell bodies of the sensory neurons in question are located within the brainstem and are intermingled With the motor cells. Leinfelder and Black (’42) suggest that proprioceptive impulses may originate in other tissues than the extraocular muscles and their tendons. Tenon’s capsule is listed as a possibility for such nerve endings.


Proprioceptive fibers for the oculomotor nerve may have an origin similar to those of the trochlear nerve. The origin for those of the abducens nerve is a little more difficult to explain. While it seems to the author that cells of the mesencephalic V type offer the most likely source of proprioceptive fibers for the extrinsic ocular muscles, other possibilities should be examined. Perhaps there are patterns of proprioceptive conduction entirely different from those we now understand. Is it possible that motor nerves, as we know them, may play some part in this function“?

Summary

The nucleus of the trochlear nerve in human embryos and fetuses is formed by a main mass of cells and often by an additional smaller mass of cells which lies farther caudad. This caudal group of cells may be bilateral or unilateral. When it is unilateral, it may occur on either the right or the left side. The size of the main nuclear group is often in inverse proportion to the size of the caudal group. Small cells are scattered along the course of the trochlear nerve Within the brain during certain stages of development. Sometimes these cells form a distinct cluster.

Occasional cells of the mesencephalic fifth type occur in the main nucleus of the trochlear nerve. These cells are easily recognized in older fetuses. They also occur in relation to the course of the trochlear nerve within the brain. The processes of some of these cells extend among the fibers of the trochlear nerve.

The cou1'se of the trochlear nerve at one point lies in close relation to the mesencephalic root of the fifth nerve. It is difficult to determine to what extent there is an exchange of fibers. The trigeminal nerve contributes fibers to the trochlear nerve along its peripheral course. Some of these fibers

accompany the trochlear nerve toward the brain and are lost in the meninges.

Literature Cited

AR1i:'Ns KAPPERS, C. U., G. C. HUBER AND E. C. CROSBY 1936 The comparative anatomy of the nervous system of verteberates, including man. The Macmillan Co., New York.

CORBIN, K. B. 1940 Observations of the peripheral distribution of fibers arising in the mesencephalic nucleus of the fifth cranial nerve. J. Comp. Neur., vol. 73, pp. 153-177.

Comanv, K. B., AND F. HARRISON 1940 Function of mesencephalic root of fifth cranial nerve. J. Nenrophysio1., vol. 3, pp. 4234135.

1942 Further attempts to trace the origin of afferent nerves to the extrinsic eye muscles. J. Comp. Neur., vol. 77, pp. 187~190.

CORBIN, K. B., AND R. K. OLIVER 1942 The origin of fibers to the grape-like endings in the insertion third of the extra-ocular muscles. J. Comp. Neur., vol. 77, pp. 171—186.

FREEMAN W. 1927 The columnar arrangement of the primary afferent centers in the brain-stem of man. J. Nerv. and Ment. Dis., vol. 65, pp. 378——397.

GEHCCHTEN, A. VAN 1903 Recherches sur 1’origine réelle et le trajet intracérebral des nerfs moteurs par la méthode de la dégénérescence wallérienne indirecte. Le Névraxe, vol. 5, pp. 265-337.

GOLGI, C. 1893 Interim a1l’origine del quarto nervo cerebrale. Arch. Ital. de Biologie, vol., 19. (Quoted from Freeman.)

1117131112, G. C. 1900 Sensory nerve terminations in the tendons of the extrinsic eye~muscles of the cat. J. Comp. Neur., vol. 10, pp. 152-158.

LEINFELDER, P. J ., AND N. M. BLACK, JR. 1942 Experimental transposition of extraocular muscles in monkeys. Amer. J. 0phth._. vol. 25, pp. 974-976.

Pearson AA. The development of the nervus terminali in man. (1941) J. Comp. Neurol. 75: 39-66.


Pearson AA. The development of the olfactory nerve in man. (1941) J. Comp. Neurol. 199-217.

SABIN, F. R. 1901 An atlas of the medulla and midbrain. The Friedenwald Co., Baltimore, Md.

SANO, F. 1941 fiber die zwei order mehrfache Teilung des Trochleariskerns beim Menschen und einigen Saugetieren. Tokyo Igakkwai Zassi, vol. 55, pp. 490-497.

TARKHAN, A. A. 1934 The innervation of the extrinsic ocular muscles. J. Anat., vol. 68, pp. 293—313.

TOZER, F. M. 1912 On the presence of ganglion cells in the roots of the III, IV, and VI cranial nerves. J. Physiol., vol. 45. Proc. Physiol. Soc., p. XV.

Toznn, F. M., AND C. S. SHERRJNGTON 1910 Receptors and afferents of the third, fourth and sixth cranial nerves. Proc. Roy. Soc., London, Ser. l-3,. vol. 82, pp. 450-457.

TSUCHIDA, U. 1906 Ueber die Ursprungskerne der Augenbewegungsnerven und fiber die mit diesen in Beziehung stehenden Bahnen im Mittel« und Zwischenhirn. Arb. a.. d. hirnanat. Inst. in Ziirich, Bd. 2, S. 1. (Quoted from Ariéns Kappers, Huber and Crosby.)

VAN VALKENBURG, C. T. 1912 On the splitting of the nucleus trochlearis. Kon. Akad. v. Wetensch. te Amsterdam, Proc. sect. sc., vol. 14, pt. 2, p. 1023.

WEINBERG, E. 1928 The mesencephalic root of the fifth nerve. J. Comp. New-., vol. 46, pp. 249-405.

WINDLE, W. F. 1932a The neurofibrillar structure of the 7-mm. cat embryo. J. Comp. Neur., vol. 55, pp. 99-138.

1932b The neurofibrillar structures of the five-and-one-half-millr meter cat embryo. J. Comp. Neur., vol. 55, pp. 315—331.

ZAHAJSZKY, E. VON 1940 Beitréige zur Kenntnis der Entvvickelung des N. ocula motorius, des N. trochlearis und des motorischen N. trigeminus. Anat. Anz., Bd. 89, S. 316-332.



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