Paper - Development of the human mesencephalic trigeminal root and related neurons

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Windle WF. and Fitzgerald JE. Development of the human mesencephalic trigeminal root and related neurons. (1942) J. Comp. Neurol., 77: 597-608.

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Note this paper was published in 1942 and our understanding related to neural development has improved since this historic human study.


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Development Of The Human Mesencephalic Trigeminal Root And Related Neurons

William F. Windle and James E. Fitzgerald

Anatomical Laboratories, Northwestern University Medical School, Chicago, Illinois

Department of Obstetrics and Gynecology.


All jnxtagresial tracts and cell groups of the adult brain stem arise early in embryonic life. The meseneephalic root of the trigeminal nerve is no exception. It has its genesis late in the fourth or early in the fifth week in the human metencephalon, but not until the sixth Week ca11 it be found in the mesencephalon. By 7 weeks, the root and its nucleus have attained most of tlie characteristics of the adult. In order to understand the early development of this group of neurons, it is necessary to examine the formation of motor and sensory trigeminal roots and to pay attention to certain nerve fibers which are closely related to the mesencephalic trigeminal root during the formative period.


A series of human embryos, 4 to 7 weeks old, served for the developmental study of the rnesencephalic root and related neurons. To supplement these, a number of cat embryos, comparable with early stages in the development of man, were used. All specimens were prepared by the pyridine silver technique of Ranson. They are listed in table 1.


Growing nerve fibers, tracts and collections of nerve cells were differentially stained by the pyridine silver method, and it has been possible to plot their courses and positions on strawboard models and on graphic reconstructions with a fair degree of accuracy. It should be borne in mind that the following descriptions apply to neurofibrillar development, and that the material revealed little or nothing of possible growth and migrations of undifferentiated neuroblasts before neurofibrils have begun to form in them.


‘Expenses of this investigation were defrayed in part by grants from The John and Mary R. Markle Foundation. Part of the study was conducted at Memphis during the summer of 1942, where one of the authors was a guest of Dr. Kendall B. Corbin in the Anatomical Laboratories of the University of Tennesse.


Table 1 Specimens used for the embryological study

ClC0\VN-RUMP E§l‘Il{.-\'I'ED


SPECIES N0. LENGTH 1 AGE 2 REMARKS (mm) (days) feat 846.1 2-3 (16) 10 somites ‘cut 841.1 3-4 (17) 22 somites 4th<cat 845.4 4-5 (17+) 27 somites cat , 845.1 4-5 (17+) 33 somites ,5 ' cat 845.2 4-5 (17+) 33 somites 3 [man 821. 4 26 c I [eat 403.1 5.5 (13) 40 somites § 'eat 403.2 6 (18) 40? somites 2 cat 361.1 7 (19) '3. 5th cat 361.2 7 (19) 1’ man 828 6+ 31 38 somites 0 man 813 i 8 35 § man 864 8 35

man 912 8.8 36 35.5 days after coitus

‘"‘ man 819 9+ 37 ,3 6th man 867 10 33 . . . . E man 808 11 40 41 days after coitus 3 man 836 11+ 41

0 [man 733 11+ 41

0 g man 794 12-13 43 S man 807 12-13 43 man 840 14-15 46 . . . . 7th man 731 15+ 47 -17 days after coitus man 698 16 48

man 766 18 50

Linnn I 725 18 50

‘Measured before fixation; lengths after fixation are 1 or 2 mm. less, depending upon age.

‘ Numbers in parentheses are days after first controlled matings of cats. Ages of human embryos were estimated from length, using Arey’s (’40) table. In addition to those for which dates of intercourse are known, menstrual histories were obtained in ten instances. When 14 days are subtracted from the onset of menstruation, all times but one agree within 6 days of the assigned age; four of the times agree within 1 to 3 days.


Observations

From forth week

Motor and sensory trigeminal roots begin to develop during the fourth week. A few neurons of the primordial semilunar ganglion are present in the 4mm. embryo, but no root fibers have reached the brain. The motor root arises from a column of cells adjacent to the floor plate, as Beccari first reported for mammals in 1923. The root fibers pass dorsolaterad in the marginal layer to emerge from the lateral aspect of the basal plate of the metencephalon. No nerve cells are present at the point of emergence. No mesencephalic root is present. A similar picture is seen in cat embryos 2mm. to 4mm. long (10 to 27 somites). In cat embryos slightly larger (33 somites, and one embryo of about 40 somites), only an occasional nerve fiber of the trigeminal sensory root has reached the brain and no spinal tract is formed. However, a small lateral longitudinal tract 3 is present at this location. It arises from a column of neuroblasts paralleling the sulcus limitans and extending rostrally as far as the isthmus between metencephalonand mesencephalon, but no farther. Several fibers descending in this tract emerge from the brain, passing into the roots of the trigeminal nerve. These may be the first mesencephalic root fibers.


Fifth week

During the early part of the fifth week, in a human embryo of 6+ mm., sensory trigerninal root fibers have entered the metencephalon opposite the sulcus limitans and have built a very short ascending, and a longer and larger descending spinal tract on the periphery of the brain. The ascending fascicle lies on the surface of the lateral longitudinal tract and its fibers merge with the latter. The lateral longitudinal tract shifts ventromesad as it passes in a caudad direction across the entering trigeminal root. The trigeminal motor root courses through bundles of the lateral longitudinal tract medial to the sensory root. Both trigeminal roots receive a few fibers from this composite tract, and these belong to the mesencephalic root.

  • We are using the term, lateral longitudinal tract, to designate the primitive compound fascicle which comprises the rnesencephalic root, Probst’s tract, part of the central tegmental bundle, and perhaps some other fibers in older stages.


Most of the trigeminal motor root fibers arise from cells of a column adjacent to the floor plate, constituting the medial motor nucleus. Other elongated motor—type cells are encountered all along the intramedullary course of the motor rootlets. These cells evidently developed their neurofibrils While migrating laterad from the medial cell column. A small group of them can be seen dorsally in the angle between emerging motor root and entering sensory root, especially toward the rostral end of the trigeminal region. It does not constitute the primordium of the definitive special visceral motor nucleus of the trigeminal nerve, as We shall see later, but appears to be, in part, the precursor of a dorsal motor nucleus (Van Valkenburg, ’10). This group of cells merges With the columnar nucleus of the lateral longitudinal tract. The relationship there suggests a contribution of cells to the caudal part of the nucleus of the lateral longitudinal tract, and it is from the nucleus of the lateral longitudinal tract that the mesencephalic root nucleus and apparently the nucleus of the locus caeruleus take origin.


In cat embryos about 7 mm. long, little evidence of a lateral migration of motor cells can be found. Here and there, an elongated neuroblast is present among the intramedullary motor rootlets of the trigeminal nerve. A small group of neurons is located in the angle between motor and sensory roots; some appear to be interneurons but others send their axons out of the brain With the trigeminal nerve roots. Perhaps cells With dorsal motor nucleus potentialities migrated before their neurofibrils formed, in the cat.


The mesencephalic root of the trigeminal nerve of the 6+ mm. human embryo arises as part of the lateral longitudinal tract. This composite tract begins at the isthmus and descends into the tegmentum of the myelencephalon. In sections just above the trigeminal root level, large cells contribute axons to its more dorsomedial border. These axons pass into the ascending sensory, and the motor trigeminal roots as mesencephalic root fibers; the rest of the lateral longitudinal tract, containing many fibers taking origin nearer the isthmus, shifts mesad to cross the trigeminal roots and continues caudad into the tegmentum medial to the trigeminal spinal tract. At least a part of this larger portion of the lateral longitudinal tract seems to constitute the tract of Probst, whose cells of origin may be the primordium of the nucleus of the locus caeruleus.


Secondary neurons forming the primordia of trigeminal sensory nuclei can be differentiated from the cell group forming the dorsal motor nucleus and locus caeruleus nucleus. They stain less heavily, are oriented differently, and their axons are thinner; many course through the marginal layer and floor plate to enter into the composition of a Ventral longitudinal tract on the opposite side (Rhines and Windle, ’41). Rostral to the trigeminal region, secondary neurons arise more dorsally in the alar plate where that structure enlarges to form the primordium of the cerebellum. They lie dorsal to the cells of the lateral longitudinal tract, and their axons pass ventrad as the first cerebellar efferents——a flocculo-tegmental system of neurons. Many, if not all, of these fibers cross the floor plate and enter the opposite reticular formation.


By the end of the fifth week, in 8 mm. embryos, it is possible to differentiate structures in the trigeminal region more clearly. Migration of nerve cells along the intramedullary trigeminal motor rootlets is still in progress, but the medial motor nucleus has not diminished in size. In fact, it is much larger than it was a few days earlier. A group of neurons in the angle between motor and sensory trigeminal roots is the dorsal motor nucleus. Rostrally these cells adjoin those of the nuclei whose axons build the lateral longitudinal tract. This tract is found no farther rostrally than the trochlear nerve. The more deeply situated fibers comprise the mesencephalic root and pass into the ascending sensory tract of tlie trii geminal nerve. They arise from rather large cells in the common nucleus of the lateral longitudinal tract as far rostrally in the meteneephalon as a point midway between the trigeminal nerve and the isthmus.


Sixth week

During the first half of the sixth week, in embryos 8.8 mm. to 10 mm. long, a reduction in number of migrating motor neurons can" be observed. Only in the more rostral fascicles of the intramedullary motor root are any of these cells present. The medial motor nucleus has attained its maximum development. A few cells ventral to the exit of the motor root can be considered to be the beginning of the definitive special visceral motor nucleus. Th.e dorsal motor nucleus is a little smaller than the salivatory nucleus of the facial nerve and is in alignment with the latter. Its axons can be followed into the motor, and especially the sensory trigeminal roots. The cells themselves appear to be a little smaller than most of those in the main, medially placed motor nucleus. The dorsal motor nucleus lies dorsomcdial to the angle between the emerging motor root and the peripherally placed primary afferent trigeminal tract. When followed rostrad, this nucleus is continuous with the group of cells thought to be locus eaeruleus.


In the lateral part of the latter, large argyrophilic cells begin to appear opposite the middle third of the ascending sensory root of the trigeminal nerve. These clearly are neurons of themesencephalic root. ‘The tract joins the ascending sensory root atthis place. Axons of smaller cells course with the mesencephalic root fibers. They contribute to Probst’s tract which is incorporated in the common lateral longitudinal tract with the mesencephalic root at this stage. This common tract shifts dorsomesad away from the ascending sensory root as it is followed in a rostral direction. It appear as a prominent flat bundle until the level of the trochlear nerve is reached. Few fibers of the mesencephalic root are found rostral to the trochlear nerve and all of the large argyrophilic cells lie caudal to it.


Axons of the cells thought to comprise the locus caeruleus pass into the marginal layer of the basal plate just medial to the exit of the motor trigeminal root. This nucleus begins to show a ventromedial relationship to the mesencephalic nucleus throughout the metencephalon in 10 mm. embryos. Consequently at the upper part of the ascending sensory root of the trigeminal nerve, some of its fibers intervene between the ascending sensory and mesencephalic root proper. In 10 mm. embryos, the vestibular nerve sends a small bundle of fibers toward the primordium of the cerebellum. These lie superficial to the thin fibers arising in the flocculus, and are superficial and dorsal to the mesencephalic root and Probst’s tract.


During the latter part of the sixth week, in embryos 11 mm. to 12 mm. long, the mesencephalic root and associated fibers can be observed in the mesencephalon rostral to the trochlear nerve. Large cells of origin are much more numerous in the metencephalon, however. The mesencephalic root passes caudad along the lateral mesencephalic wall toward the isthmus where it comes to lie more dorsally. As it (with Probst’s tract) crosses the intramedullary root of the trochlear nerve it lies superficial to the dorsal one—third of the trochlear root. There a few mesencephalic root— or associated _fibers turn mesad into the intramedullary root of the trochlear nerve and pass toward the decussation. At this place, about the same number of fibers leave the trochlear root and turn caudad i11to the mesencephalic root or Probst’s tract. Thus there is a partial decussation of the rostral portion of the mesencephalic root and (or) its associated fibers in the crossing of the trochlear nerve. These fibers comprise less than 5% of the trochlear decussation. Fabre and Mégevand (’41) have observed this decussation, which they attribute to a tecto—bulbar tract in the chick, and Shaner (’32) saw an interchange of fibers with the trochlear nerve in pig fetuses. Biondi (’13) seems to have been the first to describe a crossing of mesencephalic root neurons.


The mesencephalic root continues to course caudad, increasing in size in the metencephalon. It enters the deep border of the ascending sensory trigeminal root and presumably leaves the brain with it. An exchange of trigeminal sensory and motor fibers within the brain, as well as just after the motor root emerges, can be observed. fibers from the region of the locus caeruleus are still intimately related to the mesencephalic root above the trigeminal level. Most of them shift ventrad into the lateral part of the reticular formation as Probst’s tract, which helps form the compact lateral longitudinal tract, and can be followed caudad in sections between the trigeminal and facial levels.


At the end of the sixth week, the dorsal motor nucleus of the trigeminal nerve is not seen so clearly as in the younger embryos, because planes of section are not so favorable and because the number of obscuring interneurons has increased. There has been a change in other motor components. At this stage (11 mm. to 12 mm.) only a few motor cells are encountered in the medial position along the floor plate. A large motor nucleus is now found in a lateral position medial to the point of emergence of the motor root. This is the definitive trigeminal motor nucleus, distinct from the dorsal nucleus which was formed at the 6 mm. to 8mm. stages. A few thin axons can be traced back mesad from the definitive motor nucleus to the region formerly occupied by it (the medial motor nucleus). Some of them form a minute genu there, retracing the course taken by the migration which formed the lateral motor nucleus. However, most of trigeminal motor neurons must have shifted positioii without leaving any trace of the course they took, for this genu is much smaller than the intramedullary motor roots were in younger embryos. It is not so prominent as that observed in the cat (Windle, ’33).

Seventh. week

During the seventh week, in embryos 13 mm. to 18 mm. long, the mesencephalic root of the trigeminal nerve undergoes no changes other than to increase in size. Its cells of origin become distinct in the lateral mesencephalic wall. The apparent decussation contains more fibers but still forms only a small fraction of the intramedullary trochlear nerve root. As it joins the deep border of the ascending sensory trigeminal nerve root, the mesencephalic root sends a bundle of fibers (apparently collaterals) ventromesad into the rostral part of the main lateral motor trigeminal nucleus (Biondi, ’13). The formation of this reflex connection at the middle of the seventh week is the last step in differentiation of this tract.


Probst’s tract arises in common with the mesencephalic root in the metencephalon; perhaps a few fibers are contributed to it rostral to the isthmus. Its fibers can be difierentiated from the mesencephalic root only by observing their origin from smaller, less argyrophilic cells, and their course caudal to the trigeminal nerve Where they lie medial. to the spinal tract of the trigeminal nerve in the lateral longitudinal tract.

Discussion

In earlier studies in the cat (Windle, ’32 a,b; ’33) the composite nature of the lateral longitudinal fascicle in the rostral nietencephalon was recognized, but not fully appreciated. It was reported that fibers closely related to the mesencephalic root (they were designated tecto-bulbar) pass into the reticular formation caudal to the trigeminal level. Other investigators (Biondi, ’13; Shaner, ’23; Castaldi, ’23, ’24, ’26) apparently experienced similar difliculty in recognizing the true nature of this system. In the rabbit, Kimmel (’41) saw that many of these fibers descend caudal to the trigeminal level, but he believed them all to be mesencephalic root fibers. W'e believe that the fibers descending caudal to the trigeminal nerve are interneurons, constituting what appears to be Probst’s tract and perhaps other descending tracts of the lateral pontile tegmentum.


We have not been able to confirm Kimmel’s observation that some of these neurons emerge with the facial nerve. In the present series of silver stained ‘embryos We can observe mesencephalic root neurons entering no nerve roots except the trigeminal, and perhaps the trochlear. The relationship of the lateral longitudinal tract (containing the mesencephalic root) to the trochlear decussation is suggestive of a contribution to that nerve but there is no proof that they leave the brain with it. About as many fibers swing into the trochlear commissure from the midbrain as pass out of it into the metencephalon, a point which favors the present conclusion that a decussation of descending fibers, either meseneeplialic root or closely related neurons, occurs wit.h the motor fascicles of the trochlear nerve.


In an experimental study of the cat, Corbin (’42) found no evidence for origin of Probst’s tract in the locus caeruleus nucleus but, on the other hand, he did not entirely exclude this nucleus as a source of some of the more caudal fibers. In the embryologic material it is uncertain that cells giving‘ rise to the tract of Probst will become the locus caeruleus nucleus, but their relation to the mesencephalic root neurons is suggestive of this. The cells are unlike the large 1nesencephalic neurons. They may, however, become the smaller elements before the adult stage is reached. Until the course of fibers known to arise in the adult locus caeruleus nucleus is determined, the question of their contribution to Probst’s tract will remain unsettled.


The decussation of mesencephalic root or related neurons in the anterior medullary velum with the trochlear nerve is a prominent feature of human embryo brains. That Corbin (’42) did not find degenerating fibers in this location may indicate that they remain unmyelinated in the adult eat. It is probable that they are more conspicuous in the embryo than they are in the adult, becoming rudimentary in the course of development.


Development of the cells of the mesencephalic nucleus deserves passing comment. They are unlike the afferent neurons of cranio-spinal ganglia in one respect. The latter assume a bipolar character very early a.nd much later attain unipolarity.


The mesencephalic neurons are unipolar from the earliest stage at which they can be recognized definitely. They are like all neural tube neuroblasts in this respect, a11d differ from motor and interneurons by failing to send out dendritic processes. That they arise from the neural crest or even from alar plate elements can not be determined in the human and cat embryos of our series. A possibility that some of them come from migratory trigeminal motor neuroblasts in human embryos has been suggested. A derivation of afferent neurons from primary efferent elements may not be unique, for evidence of the presence of proprioceptive neurons in the oculomotor nucleus of the cat has been obtained (Corbin and Harrison, personal communication).

Summary

The trigeminal mesencephalic root has its genesis in a lateral longitudinal faseicle in common with Probst’s tract and other descending fibers. At 6+ mm. this common lateral longitudinal faseicle arises from a column of cells extending along the sulcus limitans from the isthmus caudalward. At the trigeminal level this cell column is coextensive with a dorsal motor nucleus which arises by lateral migration of cells along intramedullary trigeminal motor rootlets. 3-Iesencephalic and locus caeruleus nuclei may take origin in part from this early motor migration. The definitive trigeminal motor (special visceral) nucleus arises between 10mm. and 12 mm. by a second migration in which a rudimentary genu is formed, as in the facial nerve.


Probst’s tract and the mesencephalic root lie together between the central tegmental tract and the ascending afferent trigeminal ramus in 8 mm. to 10 mm. embryos. As the mesencephalic root fibers enter the trigeminal nerve, Probst’s tract continues caudad. The mesencephalic root nucleus differentiates in a caudo—rostral direction. Its cells appear just rostral to the trigeminal nerve at 81nm., reaching the isthmus at 10 mm., and the mesencephalon between 10 mm. and 12 mm. A few fibers of the mesencephalio root or related tracts decussate in the isthmus with the trochlear nerve. Reflex collaterals enter the trigeminal motor nucleus at 16 mm.

Literature Cited

AREY, L. B. 1940 Developmental anatomy, Philadelphia, W. B. Saunders (ref. on p. 131).

BECCARI, N. 1923 Intorno al primo differenziamento dei nuclei motori dei nervi cranici. Monitore zool. ital., vol. 34, pp. 161-166.

BIONDI, G. 1913 I nuclei d’origine e terminali del nervo trigemino nel pollo. Riv. ital. neuropat., psich, elettrothen, vol. 6, p. 49-57, 117-129.

COKBIN, K. B. 1942 Probst’s tract in the cat. J. Comp. Neur., vol. 77, pp. 455-467.

CASTALDI, L. 1923-1926 Studi sulla struttura e sulla sviluppo del mesencefalo. Rieerche in Cavia cobaya. Arch. ital. anat. embriol., vols. 20, 21, 23, pp. 23-225, 172-263, 481-609.

FABRE, J., AND A. MEGEVAND 1941 Développement du nerf pathétique chez Pembryon dc poulet. Comp. rend. soc. physique et d’hist. natur., Genéve vol. 58, pp. 79-81.

KIMMEL, D. L. 1941 Development of the afferent components of the facial, glossopharyngeal and vagus nerves in the rabbit embryo. J. Comp. Neur., vol. 74, p. 447-471.

R-HINES, RUTH, AND W. F. VVINDLE 1941 The early development of the fussciculus longitudinalis medialis and associated secondary neurons in the rat, cat and man. J. Comp. Neur., vol. 75, pp. 165-189.

SHAKER, R. F. 1932 The development of the nuclei and tracts of the midbrain. J. Comp. Ne-.ur., vol. 55, pp. 493-511.

VAN VALKENBUILG, C. T. 1910 Nucleus facialis, nucleus trigemini posterior, nucleus trochlearis posterior. Kon. Akad. v. Wetensch. te Amsterdam, Proc. sect. sc., vol. 13, pt. 1, pp. 143-148.

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

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

1933 Neurofibrillar development in the central nervous system of cat embryos between 8 and 12mm. long. J. Comp. Neur., vol. 58, pp. 643-723.


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Mark Hill.jpg
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)

Reference

Windle WF. and Fitzgerald JE. Development of the human mesencephalic trigeminal root and related neurons. (1942) J. Comp. Neurol., 77: 597-608.


Cite this page: Hill, M.A. (2019, August 20) Embryology Paper - Development of the human mesencephalic trigeminal root and related neurons. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Development_of_the_human_mesencephalic_trigeminal_root_and_related_neurons

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