Paper - The trochlear nerve in human fetuses (1943)
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The Trochlear Nerve in Human Fetuses
Anthony A. Pearson
Loyola University School of Medicine, Chicago, Illinois
Ten Figures (1943)
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.
aq.cer., or cer.aq., aquaeductus cerebri
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.
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.
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“?
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.
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