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| | #REDIRECT [[Paper - The trochlear nerve in human fetuses (1943)]] |
| {{Ref-Pearson1943}}
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| {| class="wikitable mw-collapsible mw-collapsed"
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| | [[File:Mark_Hill.jpg|90px|left]] This historic 1943 paper by Pearson described development of the fetal human trochlear nerve.
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| <br>
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| '''Modern Notes'''
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| {{Neural Links}}
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| <br>
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| [https://www.ncbi.nlm.nih.gov/pubmed/?term=trochlear+nerve+development Search PubMed trochlear nerve development] | |
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| {{Historic Disclaimer}}
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| =The Trochlear Nerve in Human Fetuses=
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| Anthony A. Pearson
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| Loyola University School of Medicine, Chicago, Illinois
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| TEN FIGURES (1943)
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| INTRODUCTION
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| The early development of the trochlear nerve in mammalian
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| embryos has been described by Windle (’32 a, ’32 b),
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| Zahajszky ( ’40), and others. The discussion will be limited to
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| the later development of the trochlear nerve and its relation
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| to the trigeminal nerve.‘ This study is based on serial sections
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| of human embryos and fetuses stained with various silver
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| methods. The whole heads of the smaller fetuses and em—
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| bryos were sectioned and studied; however, only the brains of
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| the larger fetuses were prepared. Most of the material used
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| in this study has been listed in previous papers (Pearson,
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| ’41 a, ’41 b) and only necessary data will be given here.
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| NUCLEUS OF ORIGIN
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| The nucleus of the trochlear nerve is easily recognized in
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| older human embryos and fetuses as a large mass of multipolar neurons located just caudal to the nucleus of the oculo—
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| motor nerve. There is no wide interval between the nuclei of
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| the third and fourth cranial nerves. A distinct thinning out
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| of the cells of the motor column, however, indicates a boundary
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| between the nuclei of these two nerves. The trochlear nucleus
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| is in line with the lateral groups of cells of the oculomotor
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| nucleus. It is located i11 its characteristic position, dorsal to
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| and partly imbedded in the medial longitudinal fasciculus.
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| The nucleus of the trochlear nerve is formed by one main
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| mass of cells and sometimes by an additional smaller mass of cells which lies farther caudad (figs. 1, 2, 3). The caudal group
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| of cells may be bilateral or unilateral. VVhen it is unilateral,
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| it may occur on either the right _or the left side.
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| This subdivision of the trochlear nucleus into a larger
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| cephalic portion and a smaller caudal portion has been observed by several investigators (Sabin, ’O1; Tsuchida, ’06;
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| van Valkenburg, ’12; and Sano, ’41). Tsuchida reported a subdivision in the trochlear nucleus in some 20 to 30% of the
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| brainstems studied, this differentiation occurring in most of
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| the specimens on only one side. In the material studied‘ by
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| the author the percentages were somewhat higher. The caudal
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| division of the trochlear nucleus occurred nearly as often on both sides as on only one side. When the caudal division was
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| present on one side only, it was found to occur about as frequently on the right side as on the left side.
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| ABBREVIATIONS
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| aq.cer., or cer.aq., aquaeductus cerebri
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| cer., cerebellum
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| c.mes.V., cells of the mesencephalic root
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| /of V
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| dcc.N.IV, decussation of the trochlear
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| nerve
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| f.1.m., fasciculus longitudinalis medialis
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| 4th vent., fourth ventricle
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| gang.N.V, ganglion semilunare
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| med.ob1., medulla oblongata
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| me.root V, mesencephalic root of the
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| trigeminal nerve
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| mes.V et nu., mesencephalic root of V
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| and nucleus
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| N.III, nervus oculomotorius
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| N .IV, ncrvus trochlearis
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| N.V, nervus trigeminus
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| nu.IV, nucleus nervi trochlearis
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| nu.IV p.caud., nucleus trochlearis (pars
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| caudali)
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| V., or vent., ventriculus
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| X, 3. group of cells in the path of the
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| trochlear nerve
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|
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| Fig. 1 A agittal section through the brainstem of a 29-mm. human fetus
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| (no. 29). Note the rostral and caudal divisions of the trochlear nucleus. Copper protargol preparation (section 16-1-2). X 12.
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| Fig. 2 A transverse section through the mesencephalon of a 5-month-old fetus
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| (no. 64) at the level of the main nucleus of the trochlear nerve. In the left nucleus
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| of the IV nerve there are two cells of the mesencephalic V type. Pyridine silver
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| preparation (section 29-3-4). X 24.
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| In one human fetus of about 5 months of age (no. 63) the
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| trochlear nucleus on each side was a single mass of cells. In another fetus (no. 64) of about the same age, there was a
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| caudal division of the trochlear nucleus on each side (fig. 3).
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| This caudal division was a small group of darkly staining
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| Inultipolar neurons. It was located about 1 mm. caudal to the
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| Fig. 3 A transverse section through the mesencephalon of a 5-month-old fetus
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| (no. 64) at the level of the caudal division of the trochlear nucleus. Pyridine silver
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| preparation (section 24-3-3). X 24.
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| main nucleus and was approximately 0.2 mm. in length. This
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| caudal nucleus of the trochlear nerve was slightly smaller on
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| the right side than on the left. There are about sixty cells
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| in the caudal nucleus on the right side and about eighty-three
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| cells on the left side. This is only an approximation, as the
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| cells were closely packed and it was difficult to make an exact count. In the fetus which possessed only the main nucleus
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| of the trochlear nerve it is interesting to note that this main
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| nucleus measured slightly more than 1 mm. in length and was
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| quite symmetrical. In the other fetus of this same age, tl1e
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| main nucleus measured less than 1 mm. in length. On the right
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| side, the main nucleus was about 0.9 mm. in length and the
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| caudal division contained about sixty cells. The main nucleus
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| of the trochlear nerve on the left side measured about 0.6 mm.
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| and the caudal division contained about eighty—three cells.
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| The cross sectional area of the main nuclei of the trochlear
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| nerve in both fetuses appeared to be approximately equal.
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| These two fetuses are thought to be fair examples of the
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| cellular arrangement of the trochlear nerve nuclei. This suggests that the size of the main nucleus is in inverse proportion
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| to the size of the caudal division. There is no indication that
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| the fiber connections of the caudal division are any different
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| from those of the main nucleus of the trochlear nerve nor is
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| there any apparent physiological significance to the separation
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| of the cells of the trochlear nerve into groups.
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| A few cells of the mesencephalic V type were observed in the
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| main nucleus of the trochlear nerve (fig. 2, left). These cells
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| are easily distinguished from the usual multipolar neurons
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| of the trochlear nucleus by their shape and size. Weinbe1'g'
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| (’28) has made a similar observation.
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| In certain embryos, scattered cells have been observed along
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| the course of the trochlear nerve central to its" decussation
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| (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
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| human fetus, such a group was found in the central course
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| of the trochlear nerve on each side (fig. 5). This group is
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| located dorsolateral to the medial longitudinal fasciculus and
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| at a plane slightly caudal to the level of the trochlear nuclei.
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| Some of the cells appear to be bipolar, although their exact
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| shapes are not distinct. Sabin (’01) has also reported the
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| presence of groups of cells along the root fibers of the trochlear
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| nerve.
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| Fig. 4 A sagittal section through the brainstem of a 17-mm. human embryo
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| (no. 16). Scattered cells are shown along the course of the trochlear nerve.
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| Pyridine silver preparation (8—3~2). X 75.
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| cm. car,
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|
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| Fig. 5 A transverse section through the mesencephalon of 9. 63-mm. human
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| fetus (no. 57). A small cluster of cells is hown in the path of the IV nerve.
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| Copper protargol preparation (section 48—2—3). X 14.
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| THE COURSE OF THE NERVE
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| Fibers of the trochlear nerve are collected into several small
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| bundles along the dorsolateral border of the trochlear nucleus
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| toward its caudal end. When a caudal division of the trochlear
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| nucleus is present an additional bundle of fibers arises here.
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| This bundle soon joins the larger bundles of the trochlear
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| nerve. The fibers of the trochlear nerve follow an oblique
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| 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
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| course of the trochlear nerve fibers is directed caudad and
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| dorsad. The caudal course of the nerve is attributed in part
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| to the shifting forward of the cells of origin during development (Ariens Kappers, Huber, and Crosby, ’36). The fibers
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| of the trochlear nerve runalmost parallel to the mesencephalic
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| root of the trigeminal nerve for a short distance. As the fibers
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| of the trochlear nerve approach the anterior medullary velum,
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| they begin to turn toward the midline. Here they lie almost
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| perpendicular to the fibers of the mesencephalic root of the
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| trigeminal nerve. As the midline is approached, the fibers of
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| the trochlear nerve can then be traced into the ventral part of
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| the decussation of that nerve. After they pass to the other
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| side, the fibers of the trochlear nerve emerge from the decussation and make their exit from the dorsolateral surface of the
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| brainstem. No trochlear fibers were observed which failed to
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| decussa.te as van Gehuchten (’03) noted in the rat and rabbit.
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| ' The course of the trochlear nerve within the brain lies deep,
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| but close to the mesencephalic root of the trigeminal nerve and
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| the nucleus of that root. It has been suggested by several
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| authors that there are connectionsxbetween the mesencephalic
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| root of the trigeminal nerve and the trochlear nerve (Freeman,
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| ’27, Weinberg, ’28 and others). Such a connection has been
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| difficult to demonstrate or rule out. There are cells of the
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| mesencephalic V type, however, which are thought to be '
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| definitely related to the trochlear nerve. Cells of this type
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| occasionally occur -in the trochlear nucleus (fig. 2), as already
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| mentioned. There are cells of the mesencephalic V type in the
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| region lateral to the anterior medullary velum. Some of these cells appear to be connected with the trochlcar nerve. An
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| occasional cell may be found directly in the course of this
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| nerve (fig. 7). These cells may appear singly or in clusters.
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| Occasionally, a process of one of these cells may be followed
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| directly among the fibers of the trochlear nerve (fig. 8). A
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| few scattered cells of the mesencephalic V type may be found
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| in the anterior medullary Velum. An example of one of these
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| cells is shown in figure 9. A bipolar cell is shown in the anterior medullary velum lying; ventral to the fibers of the
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| trochlear nerve. A process from either end of the cell extends
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| out among the fibers of the trochlear nerve. A similar cell
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| was described by Golgi (1893). V-*'indle (’32 a) described a
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| cell which sent one branch into the trochlear nerve and
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| another branch into the mesencephalic tract of a cat.
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| Fig. 6 A diagram made from several sagittal sections of the brainstem of 2:
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| 25-mm. human embryo (no. B. 1194). Pyridine silver preparation (13-20).
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|
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| Fig. 7 A section through the trochlear nerve within the rnesencephalon. Note
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| the nerve cell in the path of the nerve. From a 5»month—old human fetus (no. 64).
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| Pyridine silver preparation (19—3—4).
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|
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|
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| Fig. 8 A transverse section through the mesencephalon of a 5-m.onth~old fetus
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| (no. 64) at the level of tl1e anterior medullary velum. Note the close relation of the
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| IV nerve to the meseneephalie root of the V nerve and its nucleus. Pyridine silver
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| preparation (section 21-3-3). X 94.
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|
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|
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| Fig. 9 A photomicrograph of a nerve cell in the anterior medullary velum
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| of a. 5—month—old human fetus (no. 63). The processes of the nerve cell extend
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| dorsally among the fibers of the troehlear nerve. Pyridine silver preparation (193—4). X 450.
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| Peripheral to the decussation in the anterior medullary
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| veluin, the fibers of the trochlear nerve leave the dorsolateral
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| surface of the brainstem grouped in one or two small bundles.
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| After leaving the brain, these fibers collect into a single small
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| trunk, which can be traced ventrad close along the surface of
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| the brainstem. Before reaching the orbit the fibers of the
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| trochlear nerve pierce the dura mater and pass forward between the layers of the tentorium cerebelli.
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| As the trochlear nerve passes forward to enter the orbit it is
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| joined by a small bundle of fibers from the ophthalmic division
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| of the trigeminal nerve. This branch of the trigeminal nerve
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| leaves the ophthalmic division just peripheral to the semilunar ganglion. It joins the trochlear nerve (figr. 10) and may
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| be followed back toward the brain. Part of these fibers are
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| thought to be distributed to the dura mater along the course
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| of the trochlear nerve. A few of them can be followed between
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| the layers of the dura mater into the 1'0/gion of the transverse
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| sinus.
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| Just peripheral to the place where the above anastomotic
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| branch joins the trochlear nerve, a short part of the course of
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| the trochlear nerve lies in intimate relationship with the
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| ophthalmic nerve. The fibers of the two nerves lie so close
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| together that it is extremely difficult to determine in serial
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| sections whether there is an exchange of fibers between them.
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| After crossing the ophthalmic nerve, the trochlear nerve may
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| be traced forward into the superior oblique muscle. The part
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| of the trochlear nerve peripheral to the place where it crosses
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| the ophthalmic nerve is larger than the part of the nerve at
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| its exit from the brain. This difference in size is sufficient to
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| lead one to conclude that the trigeminal nerve contributes
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| fibers to the distal part of the trochlear nerve.
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| The lacrimal nerve occasionally receives ‘a small branch
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| from the trochlear nerve. This contribution to the lacrimal
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| nerve is probably composed of fibers which are derived from
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| the ophthalmic nerve and which simply accompany the
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| trochlear nerve for a short distance. It has been reported
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| that the trochlear nerve occasionally sends a branch to the
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| Fig. 10 A diagram drawn from the sagittal sections of the brainstem of a
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| 36-mm. human fetus (no. 34) showing a portion of the course of the trochlear
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| nerve. Copper protargol preparation.
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| orbicularis oculi muscle (Piersol, ’30).‘ This branch, however, was not observed in any of the material studied by the
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| author. In addition to the other communicating branches
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| already mentioned, there are small filaments from the
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| cavernous plexus of nerves Which join the trochlear nerve.
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| DISCUSSION
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| The investigations of several authors (Huber, ’00; Tozer
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| and Sherrington, ’10, and others) have shown that there are sensory endings in the extrinsic muscles of the eye and that
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| these endings degenerate after cutting the third and fourth
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| cranial nerves (Tozer and Sherrington, ’10, and Tarkhan, ’34) .
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| It has been more difficult to demonstrate clearly the location
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| of the cell bodies of the sensory neurons involved.
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| The anatomical evidence submitted here would indicate that
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| the proprioceptive neurons for the superior oblique muscle are
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| of the mesencephalic V type. They are thought to be located
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| in the brainstem close to the level of the trochlear nerve. The
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| details of the connections of these neurons have been discussed,
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| and they are in general agreement with the position taken by
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| Weiriberg (’28) and Tar-khan (’34) on this question. The
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| experimental work of Freeman (’27), Tarkhan_ (’34), and
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| others strongly suggests that there are proprioceptive fibers
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| in the fourth cranial nerve. The existence of proprioceptive
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| neurons is indicated, after the removal of the orbital contents,
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| by changes in the cells of the mesencephalic nucleus at the
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| level of the trochlear nerve (Freeman, ’27). Corbin (’40)
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| states that such fibers from the mesencephalic nucleus do not
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| join the trochlear nerve extracranially from branches of the
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| trigeminal nerve. Corbin and Harrison (’40 and ’42) found
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| that no action potentials were elicited from the mesencephalic
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| root of V as a result of stretching the extrinsic muscles of the
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| eye. It was possible, however, to obtain action potentials from
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| the oculomotor nucleus and the intramedullary portion of the
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| oculomotor nerve. Corbin (’40) pointed out that if cells of the
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| mesencephalic nucleus do contribute fibers to the trochlear nerve, this contribution must come from cells located between
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| the levels of the trochlear nucleus and the decussation of that
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| nerve. It seems quite likely that the majority of the cells in
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| question may occupy this position. Tozer (’12), however,
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| found no change in the meseneephalic nucleus after cutting
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| the third and fourth cranial nerves. VVe thus have experimental evidence for and against the theory that eertainlcells
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| of the mesencephalic nucleus contribute fibers to the trochlear
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| nerve. It should be remembered that the results gained from
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| the chromatolysis of cells and the Marchi method are not always reliable and that conclusions should be made with care.
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| The more recent Work of Corbin and Oliver (’42) further
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| indicates that the extrinsic ocular muscles are not innervated
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| by the mesencephalic root of the fifth nerve. These authors
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| are of the opinion that the cell bodies of the sensory neurons
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| 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
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| tissues than the extraocular muscles and their tendons.
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| Tenon’s capsule is listed as a possibility for such nerve
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| endings.
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| Proprioceptive fibers for the oculomotor nerve may have an
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| origin similar to those of the trochlear nerve. The origin for
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| those of the abducens nerve is a little more difficult to explain.
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| While it seems to the author that cells of the mesencephalic V
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| type offer the most likely source of proprioceptive fibers for
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| the extrinsic ocular muscles, other possibilities should be examined. Perhaps there are patterns of proprioceptive conduction entirely different from those we now understand. Is
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| it possible that motor nerves, as we know them, may play
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| some part in this function“?
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| SUMMARY
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| The nucleus of the trochlear nerve in human embryos and
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| fetuses is formed by a main mass of cells and often by an | |
| additional smaller mass of cells which lies farther caudad.
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| This caudal group of cells may be bilateral or unilateral.
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| When it is unilateral, it may occur on either the right or the
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| left side. The size of the main nuclear group is often in inverse proportion to the size of the caudal group. Small cells
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| are scattered along the course of the trochlear nerve Within
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| the brain during certain stages of development. Sometimes
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| these cells form a distinct cluster.
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| Occasional cells of the mesencephalic fifth type occur in the
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| main nucleus of the trochlear nerve. These cells are easily
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| recognized in older fetuses. They also occur in relation to the
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| course of the trochlear nerve within the brain. The processes of some of these cells extend among the fibers of the trochlear
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| nerve.
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| The cou1'se of the trochlear nerve at one point lies in close
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| relation to the mesencephalic root of the fifth nerve. It is
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| difficult to determine to what extent there is an exchange of
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| fibers. The trigeminal nerve contributes fibers to the trochlear
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| nerve along its peripheral course. Some of these fibers
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| accompany the trochlear nerve toward the brain and are lost
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| in the meninges.
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| LITERATURE CITED
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| 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
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| 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.
| |
| | |
| GEIICCHTEN, 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, A. A. 19412» The development of the nervus terminalis in man. J.
| |
| Comp. Neux-., vol. 75, pp. 39-66.
| |
| 1941b The development of the olfactory nerve in man. J. Comp.
| |
| Neur., vol. 75, pp. 199-217.
| |
| PIn1>.soL, G. A. 1930 Human Anatomy. Ninth edition (Huber). J. B. Lippincott 00., Philadelphia.
| |
| | |
| SABIN, F‘. R. 1901 An atlas of the medulla and midbrain. The Friedenwald Co.,
| |
| Baltimore, Md.
| |
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| 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.
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