Paper - The oculomotor nucleus in the human fetus (1944)
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The Oculomotor Nucleus in the Human Fetus
Anthony A. Pearson
Loyola University School of Medicine, Chicago, Illinois
- After July 1, 1943, at Baylor University College of Medicine, Houston, Texas.
Nine Figures (1944)
The general features of the development of the human oculomotor nucleus have been described by Mann (’27) and its development in the later part of fetal life by Tsuchida (’06). Mann pointed out that the nuclear groups of the oculomotor nerve differentiate in human development earlier than was formerly thought (Tsuchida, ’06) and that the cellular arrangement is more easily seen in certain fetal stages than in the adult. Many adult features of the oculomotor nucleus can be shown in human fetuses of 5 and 6 months of age. The author has found that the Various nuclear groups stand out particularly well in pyridine silver preparations of fetal brains. While there have been many studies on the oculomotor nerve and its nucleus in man, the Various nuclear groups are not clearly shown in the usual preparations of the adult brain. For this reason a more detailed study of certain fetal stages is considered worthy of attention." This study is based on serial sections of human embryos and fetuses stained with the various silver methods. It will not be possible to review all of the studies on the oculomotor nerve, and only references which are pertinent to the description will be mentioned. The following references are suggested for further reading: Ariéns Kappers, Huber and Crosby (’36) ; Brouwer (’18), and Le Gros Clark (’26).'
An effort will be made to keep the terminology as simple as possible. Three main groups of cells make up the nucleus of the oculomotor nerve, as follows: a chief or lateral nucleus, which in turn is subdivided into a dorsal and a ventral portion, an Edinger—W'estphal nucleus and a median nucleus. The latter is an unpaired group of cells. Mingazzini (’28) has suggested a further subdivision of the dorsal and the ventral groups of the lateral ‘nucleus into subgroups. Although there is some evidence for this (pp. 52 and 54), there seems to be little value in making the terminology more complicated unless it has functional sig nificance.
The oculomotor nerve in mammalian embryos has its anlage in the basal plate of the mesencephalon in the region of the cephalic ﬂexure (Windle, ’32, and Zahajszky, ’40). According to Mann (’27) the nuclei of the oculomotor nerves at the 25-mm. stage of human ‘development consist of two groups of cells, still continuous with the ependyma. The groups are located just beneath the ﬂoor of the cerebral aqueduct, one on either side of the midline. At this stage there is no connection across the midline of one nucleus with the corresponding nucleus on the other side. At the 35—mm. stage of development, a median nucleus which connects the lateral nuclei has di1"l"erentiat.ed. The median group was thought to be formed by an extension or fusion across the midline of the lateral groups. As development continues, these groups become more distinct. The latter groups differentiate into dorsal and ventral parts. Mann (’27) is of the opinion that the Edinger-VVest.phal nucleus is formed from a mass of undifferentiated neuroblasts which buds out from the median nucleus, and that it is present by the 48-mm. stage of human development. Thus the main nuclear groups and subdivisions of the 'oculornotor nerve can be recognized at fairly early stages in human development. The details of these nuclear groups are better shown in the later stages of fetal life.
The nucleus of the oculomotor nerve in human fetuses of about 5 and 6 months of age is located at the level of the superior colliculus in the rostral part of the mesencephalon. This is just in front of the nucleus of the trochlear nerve. It is formed by several columns of cells which measure about 2.5 to 3 mm. in length. In the adult brain the oculomotor nucleus is approximately 5 mm. long (Benjamin, ’39). The columns of cells show characteristic groupings at the various levels of the nucleus. The cells comprising the nucleus are small, medium sized, and large multipolar neurons. The large multipola r neurons form the lateral or chief nucleus, which is represented bilaterally and makes up the greater part of the oculomotor nucleus. A group of medium sized cells located in the midplane constitutes the median nucleus. This nucleus probably corresponds to the diffuse nucleus of the midline observed by Perlia (1889). It is unpaired. There are also several groups of small cells which are located along the sides of the lateral nucleus. These groups constitute the Edinger-VV'estphal nucleus. They were first observed by Edinger (1885) in fetal brains and in the adult brain a few years later by Westpha1 (1887). The anterior median nucleus is also composed of small cells and is considered a part of the Edinger—Westphal nucleus. This is in agreement with Le Gros Clark (’26) and others.
aq. cer., aquaeductus cerebri 1111. 1at., nucleus lateralis
b. ves., blood vessel nu. lat. (p. d0r.), nucleus luteralis (pars c. mes. V, cells of the mesencephalic root of V dorsalis)
dec., decussabion of oculomotor nerve ﬁbers nu. lat. (p. ven.), nucleus lateralis
f.l.m., fasciculus longitudinalis medialis (pars ventralis)
nu. E.W., Edinger—Westphal nucleus nu. 1ned., nucleus medianus
nu. E.W. (p. lat.), Edinger—Westpl1al nu. med. ant, nucleus medianus anterior
(lateral part) N. III, nervus oculomotorius nu. E.W. (p. med.), Edinger-Westphal nu. rubcr, nucleus ruber nucleus (medial part)
Fig. 1 A transverse section through the Inesenceplialon of a 5-month-old human fetus at the level of the rostral end of the oculomotor nucleus (110. 64-36-32). Pyridine silver preparation. X 26.
For convenience of description the oculomotor nucleus may be divided into rostral, middle and caudal thirds. The small—celled groups fuse i11to a single mass of cells at the rostral end of the oculomotor nucleus and extend a little farther cephalad than the other divisions of this nucleus (ﬁg. 1). This forward extension of the small—celled groups, which is sometimes referred to as the anterior median nucleus (Perlia, 1889), forms the rostral end of the oculomotor nucleus. When this mass of small cells is followed caudad in serial sections to about the level of the middle of the rostral third of the oculomotor nucleus, it splits into a larger dorsal group (the Edinge1'—Westphal nucleus proper) and a smaller ventral group (the anterior median nucleus). In between the two is the rostral end of the large—celled group or lateral nucleus (ﬁg. 2). The anterior median nucleus extends caudad along the ventral border of the lateral nucleus through the remaining part of the rostral third of the oculomotor nucleus. The larger dorsal group of small cells forms the main part of the Edinger-Westphal nucleus. As this group of cells extends caudad it splits into a lateral and a medial part. The medial part is a narrow column of cells located close to the midline and along the medial surface of the lateral nucleus (ﬁgs. 3 and 4). It disappears in the Qaudal part of the middle third of the oculomotor nucleus. The lateral part of the Edinger-Westphal nucleus is located along the dorsal border of the lateral nucleus. This lateral part does not always extend caudad as a continuous column of cells but often is composed of isolated clusters of cells (ﬁgs. 3, 4 and 5). It also disappears in the caudal part of the middle third of the oculomotor nucleus. Le Gros Clark (’26) noted that the cell groups of the Edinger-Westphal nucleus are subject to considerable variation.
Fig. 2 A transvere section slightly caudal to the middle of the rostral third of the oculomotor nucleus of a 5-month-old human fetus. The section shows the rostral end of the lateral nucleus (no. 64-35-3-3). Pyridine silver preparation. X 26.
The fiber processes of the neurons of the small—celled groups are indistinct and difficult to follow in the material studied. The distinct nuclei are the most prominent feature of these cells, and they stand out in contrast with the faint outline of the neurons. Their nuclei usually possess a single darkly staining nucleolus. These cells appear to be embedded in a delicate meshwork of ﬁne ﬁbers. It has not been possible to trace the processes of these neurons into the rootlets of the oculomotor nerve. It has evidently been assumed, because of their position and their relation to the other nuclear groups, that they are part of the nucleus of the oculomotor nerve. Because of the character of these neurons, the assumption has been made that they are part of the autonomic nervous system.
The lateral or chief nucleus is composed of large multipolar neurons, the processes of which are sharply deﬁned and stain intensely with silver stains. The neurofibrils are darkly stained and give the neurons 3. deﬁnite form which is in contrast with the indistinct outlines of the neurons of the small—celled groups. The nuclei are lightly stained and, although not large, occupy a conspicuous place in the cells. They take an eccentric position in the neuron, and each contains a dark nucleolus. These cells are embedded in a dense network of freely branching ﬁbers. The lateral nucleus extends from a level just in front of the nucleus of the trochlear nerve almost to the rostral end of the oculomotor nucleus. The rostral end of the lateral nucleus is a single mass of cells situated between the Edinger—Westphal nucleus and the anterior median nucleus (ﬁg. 2). As the lateral nucleus is followed caudad in serial sections, it begins to separate into a dorsal and a ventral group of cells. This separation occurs at about the level of the junction of the rostral a11d middle thirds of the oculomotor nucleus. The lateral nucleus shows irregular groupings at this level (fig. 3). The dorsal part of the dorsal group contains a small mass of darkly staining niultipolar neurons. These darkly staining neurons are present for only a short distance and will not be designated as a separate group. The remaining cells of the dorsal group make up the greater part of this division of the oculomotor nucleus and extend caudad as a deﬁnite column of cells. Wliile there is no wide interval between the dorsal and ventral divisions of the lateral nucleus, the arrangement of the cells indicates a separation. At about the level of the middle of the oculoniotor nucleus the dorsal and Ventral divisions of the lateral nucleus are shown distinctly (ﬁg. 4). The medial part of the Edinger—Westphal nucleus lies close along the medial side of the lateral nucleus at this level. The dorsal part of the lateral nucleus has assumed a more rounded form in cross sections. The ventral part spreads out in a dorsoventral direction with its ventral border situated nearer the midline (ﬁgs. 5 and 6). In cross sections the lateral nuclei of the two sides form a V—shaped mass of cells partly closed at the bottom by fibers crossing the midline. Through the caudal third of the oculomotor nucleus, cells from the ventral division of the lateral nucleus become scattered ventrally among the ﬁbers of the medial longitudinal fascieulus (ﬁgs. 5 to 7). These cells are sometimes referred to as the scattered cells of the large—celled portion of the oculomotor nucleus (Benjamin, ’39). Through the greater part of the caudal third of the oculomotor nucleus. there are many ﬁbers crossing from the lateral nucleus of one side to the opposite side (ﬁgs. 5 to 7). Near the rostral end of the caudal third of the oculomotor nucleus, the dorsal part of the lateral nucleus either drops out or fuses with the ventral part of the lateral nucleus (ﬁg. 6). Through most of the caudal third of the oculamotor nucleus only the ventral part of the lateral nucleus is present. It in turn is divided into a dorsal and a ventral division (figs. 7 and 8). Thus a dorsal and a ventral division of the lateral nucleus can be identiﬁed at almost every level through the oculomotor nucleus. The lateral nucleus drops out of the field just i11 front of the rostral end of the nucleus of the trochlear nerve. It is the ventral part of the lateral nucleus of the oculomotor nucleus which is in line with the trochlear nucleus.
Fig. 3 A transverse section near the rostral end of the middle third of the oculomotor nucleus of :1 5—month.old human fetus. The dorsal part of the lateral nucleus is further subdivided into dorsal and ventral parts (no. 64-34-3-2). Pyridine silver preparations. X 26.
Fig. 4 A transverse section through the middle of the middle third of the oculomotor nucleus (human fetus no. 64-34-1-2). Pyridine silver preparation. X 26,
Fig. 5 A transverse section of the mesencephalon at the level of the junction of the middle and the caudal thirds of the oculomotor nucleus. Note that a process of a cell of the mesencephnlic V type is directed toward the oculomotor nucleus (human fetus no. 6-}-32-3-3). Pyridine silver preparation. X 26.
In the region of the junction of the rostral and middle thirds of the oculomotor nucleus there is an irregular column of large cells in the midline (ﬁg. 3). These cells probably correspond to the central nucleus of Perlia (1889). It is situated medial to the Ventral division of the lateral nucleus and has the appearance of being compressed from the lateral sides. This is an inconstant group of cells, as it does not occur in every series. It seems likely that these cells are part of the lateral nucleus but l1aVe become separated from the rest of that nucleus. The blood vessels Within the midbrain which lie on either side of the midline may be partially responsible for this separation. Le Gros Clark (’26) reports that the central nucleus is not only different in different animals but shows considerable variation in a single species. Tsuchida ( ’O6) found this group of cells to be absent in 20% of the human brains he studied. This group of cells will be regarded here as part of the lateral nuclei, the cells of which have become scattered across the midline.
Fig. 6 A transverse section slightly caudal to the preceding ﬁgure. The section passes through the caudal end of the dorsal part of the lateral nucleus (human fetus 110. 64-32-22). Pyridine silver preparation. X 26.
Through the caudal half or third of the oculomotor nucleus there is a more constant group of cells located in or near the midline. These cells probably constitute the group to which Perila (1889) referred as the diffuse nucleus of the midline. It will be referred to here as the median nucleus. The majority of the cells of the median nucleus are slightly smaller than those of the lateral nucleus. There are only a few of the larger multipolar neurons scattered among the cells of this group. The median nucleus extends as a column of cells through the greater part of the caudal half of the oculomotor nucleus. In cross sections it is seen as an unpaired rounded mass of cells in the midplane (figs. 5 to 7). Toward the caudal end of the oculomotor nucleus this mass of cells either splits or spreads out lateralward and fuses with the ventral division of the lateral cell columns. It disappears a little rostral to the caudal end of the oculomotor nucleus.
While the processes of the neurons of the median nucleus are fairly distinct, it has been possible to trace them only a short distance. The majority of the neurons of the lateral nucleus send their axons into the rootlets of the oculomotor nerve of the same side. This is particularly true of the dorsal division and the rostral half of the ventral division of the lateral nucleus (ﬁgs. 2 to 5). Some of the processes of the dorsal division pass directly to the nerve rootlets, while others can be followed through the ventral division of the lateral nucleus on their way to the rootlets of the same side. The axons of the rostral half of the ventral division and the large scattered cells of the lateral nucleus are thought to send their processes directly into the rootlets of the oculomotor nerve of the same side.
Many neurons of the caudal half of the ventral division of the lateral nucleus send their axons into the rootlets of the oculomotor nerve of the opposite side (ﬁgs. 6 and 7). The crossed ﬁbers of the oculomotor nerve appear to leave the ventral division of the lateral nucleus of one side, sweep ventrally across the midline, sweep dorsally again and through the lateral nucleus of the opposite side, and then turn ventrally into the rootlets of the oculomotor nerve (ﬁg. 7). At the very caudal end of the oculomotor nucleus, however, there appear to be no ﬁbers of the oculomotor nerve which cross the midline (ﬁg. 8). It is generally believed that at least part of the ﬁbers to the medial rectus muscles are crossed. The processes of the neurons in the median nucleus are more distinct than those of the small-celled groups, and yet it was not possible to trace their axons any great distance (ﬁgs. 5 to 7). Neither was it possible to determine whether or not the processes of any of these cells enter the roots of the oculomotor nerve. Fibers leave the lateral and Ventrolateral borders of the lateral nucleus and converge into small bundles. These form the rootlets of the oculomotor nerve and they pass Ventrad along the medial and caudomedial surfaces of the red nucleus (ﬁgs. 2 to 4). A few of the ﬁbers pass Within the medial border of that nucleus. The more caudal ﬁbers of the oculomotor nerve pass ventrad in broad curves just caudal to the red nucleus (ﬁg. 5). These ﬁbers converge into larger bundles as they make their exit from the mesen— cephalon along and partly through the medial border of the cerebral peduncle.
Fig. 7 A transverse section near the middle of the caudal third of the oculomotor nucleus (human fetus no. 64-31-3-4). Pyridine silver preparation. X 26.
As the ﬁbers of the oculomotor nerve sweep ventrally through the tegmentum of the midbrain they come i11to relation with the reticular formation in that region. The reticular formation is conspicuous in the levels just caudal to the red nucleus. It is formed of interlacing ﬁbers and neurons. Some of these neurons appear to have no relation to the roots of the oculornotor nerve, whereas in other places they appear to be strung along or to be in groups around the roots of the oculomotor nerve (ﬁg. 9). Most of these cells appear to be multipolar neurons; while a few of them appear to be bipolar cells.
There are a few cells of the mesencephalic V type in relation to the nucleus of the oculomotor nerve. Some of these cells are located just lateral or dorsolateral to the dorsal division of the lateral nucleus (ﬁg. 6). These cells often show a process directed toward the oculomotor nucleus (ﬁg. 5). Certain of the lateral rootlets of the oculomotor nerve contain ﬁbers which turn dorsolaterally toward the cells of the mesencephalic nucleus of V. Occasional cells of the mesencephalic V type occur in the oculomotor nucleus. Weinberg (’28) has made similar observations and suggests that there is a connection between the cells of the mesencephalic V type at this level and the oculomotor nucleus.
Fig. 8 A transverse section through the mesencephalon at the level of the caudal end of the oculomotor nucleus (human fetus no. 64-30-3-3). Pyridine silver preparation, X 26
Fig. 9 Cell along the intramcdullary course of rootlets of the oculomotor nerve of a 5month-old human fetus (no. 64-33-1-1). Pyridine silver preparation.
It is diﬁicult, however, to demonstrate this connection completely. A few cells of the mesencephalic V type occur in the peripheral course of the oculomotor nerve. In the older specimens where these cells were observed, only a short stump of the oculomotor nerve remained attached to the brain stem, and it was not possible to examine the whole course of the nerve. Nicholson (’24) found forty-four ganglion cells along the peripheral course of the oculomotor nerve of a human fetus.
There are many problems concerning the oculomotor nerve and its nucleus which remain unsolved. A number of attempts have been made to discover a pattern of localization within the nucleus. Bernheimer (1897) concluded that there is a cephalo-caudal arrangement of the neurons in the oculomotor nucleus for the control of the extrinsic muscles of the eye. The suggested arrangement, beginning with the rostral end, is as follows: the levator palpebrae superioris, the superior rectus, the internal rectus, the inferior oblique, and the inferior rectus muscles. Brouwer (’18) reached much the same conclusion and was of the opinion that neurons in the median nucleus send processes to the internal rectus muscle. Le Gros Clark (’26) recognized the probable validity of the last statement. He questioned, however, on the basis of comparative anatomical studies, the justification of applying to the median nucleus the term “nucleus of convergence”. The various schemes proposed for a localization within the oculomotor nucleus do not agree in detail a.nd yet they support the thesis that there is a certa.in degree of localization present. Le Gros Clark (’26) has suggested that the functional elements of the oculomotor nucleus are arranged dorsoventrally rather than cephalocaudally. He is of the opinion that the dorsal group of the lateral nucleus is concerned with upward movements of the eyes and the ventral group with downward movements. The trochlear nucleus is almost continuous with the ventral group and is also concerned with the downward movements of the eyes. Clinical evidence has shown that the median nucleus is associated with movements of the eye toward the midline (Brouwer, ’18). The outward movements of the eye are obviously taken care of by the abclucens nucleus. Thus, according to Le Gros Clark (’26), there is a localization of movements within the eye-muscle nuclei rather than of individual muscles. According to the recent experiments of Bender and VVeinstein (’43) with the Horsley-Clarke apparatus, the individual ocular muscles supplied by the third nerve are represented within the oculomotor nucleus of the same side. According to them the clorsoventral and rostrocaudal arrangement of the functional representation of the ocular muscles is as follows: sphincter pupillae, i11ferior rectus, ciliary ("!), inferior oblique, internal rectus, superior rectus, a11d levator palpebrac. A straight anatomical study gives little additional information on the problem of the localization of function within the oculomotor nucleus. This subject is still in need of clariﬁcation.
It is generally believed that the Edinger-Westphal nucleus is concerned with the innervation of the sphincter muscle of the iris and the ciliary muscles. The proof of this assumption has been diﬂicult to obtain. Crouch (’36) has concluded from experimental work on cats, that fibers from the Edinger-VVestphal nucleus pass to the orbit by way of the oculomotor nerve. These fibers were thought to be crossed and uncrossed. Benjamin (’39) reported that at least one of the functions of the Edinger—VVestphal nucleus in the cat is constriction of the pupil. He is of the opinion that the anterior median nucleus in the cat may be a part of the constrictor center.
Most investigators believe that the nucleus of Darkschewitsch gives rise to ﬁbers of the posterior commissure rather than of the oculomotor nerve (Ariéns Kappers, Huber and Crosby, ’36). Ingram and Ranson (’35) have discussed in some detail-the relations of the nucleus of Darkschewitsch and the nucleus interstitialis of Cajal. The experiments of Jones (’42) on the chick indicate that the ciliary ganglion is formed from cells which migrate along the oculomotor nerve at a very early stage of development.
There is evidence that the epilemmal grape-like endings in the insertion third of the extra—ocular muscles are proprioceptors (Corbin and Oliver, ’42, and others). There is still uncertainty concerning the origin of the ﬁbers which have these proprioceptive endings. The oculomotor nerve like the trochlear nerve (Pearson, ’43a) has cells of the mesencephalic V type related to its course. Granglion—1ike cells occur in the peripheral course of the nerve and Within its nucleus (p. 59). Certain cells of the mesencephalic nucleus at the level of the oculomotor nucleus have processes which extend toward the oculomotor nucleus. It is quite possible, as Tarkhan ( ’34:) has reported, that the processes of cells of the mesencephalic nucleus join the oculomotor nerve. As Freeman (’27) has pointed out, the number of cells of the mesencephalic nucleus is increased at the levels of the nuclei of the trochlear and the oculomotor nerves. All of this suggests a functional relationship which has been noted by a number of authors. ‘While there are a few neurons along the intramedullary course of the ﬁbers of the oculomotor nerve, these neurons are not of a distinctly sensory type like those neurons which occur along the intramedullary course of the hypoglossal nerve in the human fetus (Pearson, ’43b). The above statements indicate possible sources of proprioceptive ﬁbers within the oculomotor nerve. Corbin and Harrison (’42) obtained action potentials from the oculomotor nucleus and the intramedullary portion of the oculomotor nerve as a result of the stimulation of a branch of the oculomotor nerve. Corbin and Oliver ( ’42) are of the opinion that the cell bodies of the sensory neurons of the oculomotor nerve are located within the brain—steIn and are intermingled with the motor cells. These authors concluded that the mesencephalic root of the trigeminal nerve is not the source of the sensory ﬁbers to the extrinsic ocular muscles. They regarded the cells along the oculomotor nerve as too few in number to be the source of the fibers to the numerous grape-like endings. It is possible, however, that the cells of_ the origin of the sensory ﬁbers to the extrinsic eyemuscles are not concentrated in any one locality. When one considers the cells along the periphera.l and intramedullary course of the oculomotor nerve, within the oculomotor nucleus itself, and the cells of the mesencephalic nucleus (V) which send processes toward the oculomotor nucleus, then the number of cells may be suﬂiciently large to serve as the source of the proprioceptive ﬁbers within the oculomotor nerve.
The cell arrangement of the oculomotor nucleus in the human fetus is described. The main cell groups present in the adult brain are clearly shown in late fetal development. The cells making up the oculomotor nucleus are small, medium-sized and large multipolar neurons.
Three groups of small cells constitute the Edinger-Westpl1al nucleus. The medium.-sized cells form an unpaired group in the midline. The large multipolar neurons form the lateral nucleus which is divided into dorsal. and ventral parts. The majority of the neurons in the lateral nucleus send their axons into the oculomotor nerve of the same side. The axons of many neurons in the caudal half of the oculomotor nucleus cross the midline and pass through the nucleus of the opposite side before entering the rootlets of the oculomotor nerve. The processes of the median nucleus and the Edinger-VVestphal nucleus are much more difficult to follow.
Some of the ﬁbers of the oculomotor nerve’ are in relation to cells of the reticular formation. Cells of the mesencephalic V type are related to the oculomotor nerve. A few of these cells occur in the oculomotor nucleus and others are located along the peripheral course of the third nerve. Certain cells of the mesencephalic nucleus at the level of the oculomotor nucleus send processes toward the oculomotor nerve. These observations suggest the possible sources of proprioceptive ﬁbers in the oculomotor nerve.
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Cite this page: Hill, M.A. (2020, December 4) Embryology Paper - The oculomotor nucleus in the human fetus (1944). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_oculomotor_nucleus_in_the_human_fetus_(1944)
- © Dr Mark Hill 2020, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G