Paper - Recurrent branches of the abducens nerve in human embryos

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Bremer JL. Recurrent branches of the abducens nerve in human embryos. (1921) Amer. J Anat., 28: 371-397.

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This historic 1921 paper by Bremer describes the development of recurrent branches of the abducens nerve the sixth cranial nerve (CNVI) in human embryos.

Modern Notes: Neural - Cranial Nerve Development | Neural Crest - Cranial Nerve Development

Cranial Nerves 
Nerve Number Name Type Origin Function
CN I Olfactory sensory telencephalon smell placode
CN II Optic sensory retinal ganglial cells vision
CN III Oculomotor motor anterior midbrain extraocular muscles eye movements and pupil dilation (motor)
CN IV Trochlear motor dorsal midbrain extraocular muscles (superior oblique muscle)
CN V Trigeminal motor/sensory pons touch, mastication
CN VI Abducent motor extraocular muscles control eye movements (lateral rectus muscle)
CN VII Facial motor/sensory pons facial expression, taste (tongue anterior and central regions) regulate salivary production.
CN VIII Acoustic sensory vestibular and cochlear nuclei hearing, placode
CN IX Glossopharyngeal motor/sensory medulla swallowing and speech, taste (tongue posterior region)
CN X Vagus motor/sensory medulla larynx and pharynx muscles (speech and swallowing), regulates heartbeat, sweating, and peristalsis
CN XI Accessory motor motor neurons sternocleidomastoid and trapezius muscles
CN XII Hypoglossal motor motor neurons tongue muscles (speech, eating and other oral functions)

Cranial Nerve Links: Neural | Neural Crest | CN I | CN II | CN III| CN IV | CN V | CN VI | CN VII | CN VIII | CN IX | CN X | CN XI | CN XII | placodes | Category:Cranial Nerve
Historic Embryology Cranial Nerves 
1908 10 mm Human Embryo | 1912 Cerebral Nerves | 1925 Rat Ganglia | 1927 Oculomotor | 1938 Spinal Accessory | 1938 Hypoglossal | 1941 Olfactory | 1943 Oculomotor | 1947 Facial

Neural Links: ectoderm | neural | neural crest | ventricular | sensory | Stage 22 | gliogenesis | neural fetal | Medicine Lecture - Neural | Lecture - Ectoderm | Lecture - Neural Crest | Lab - Early Neural | neural abnormalities | folic acid | iodine deficiency | Fetal Alcohol Syndrome | neural postnatal | neural examination | Histology | Historic Neural | Category:Neural

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Recurrent Branches of the Abducens Nerve in Human Embryos

John Lewis Bremer

H armrd Medical School, Boston, Massachusetis

One Diagram and Four Figures


Recurrent branches of the abducens have been known since 1898, and their significance commented on by Neal, Platt, Dohrn, Belogolowy, and others. In an earlier paper I showed them, along with other unusual roots and branches of the abducens and hypoglossal nerves. Only recently, however, have I realized that in human embryos the recurrent branches of the abducens are to be considered normal, instead of infrequent variations, and that in man they attain their greatest frequency, size, and duration.

In many classes of vertebrates the gap along the floor of the hind—brain between the most anterior roots of the adult hypoglossal nerve and the most posterior roots of the abducens is more or less filled in the embryo by numerous ventral rootlets, some running to join the hypoglossal, caudal to the vagus and accessory nerves, some passing between the vagus and the glossopharyngeal, below the upper ganglia, others taking a more dorsal course, like the dorsal rami of spinal nerves, to end in the dorsal head musculature. Many of these rootlets are abortive, and end before their definite direction can be more than imagined. They may, if they persist long enough, cause probably transient foramina in the cartilaginous base of the skull, in line with the hypoglossal foramina, or they may pass out by the jugular foramen. They may be connected by longitudinal strands, at a short distance from their point of origin from the brain, thus forming a series of loops often continuing the direction of the abducens caudally toward the hypoglossal. Such a continuation. of the abducens caudally, or a separate caudally running root from the immediate vicinity of the permanent abduccns roots, is a true recurrent branch of the abduccns, as opposed to the other scattered rootlets more immediately connected with the hypoglossal nerve, which might be called anterior hypoglossal roots. The significance of these transient roots as a whole is the indication that the vagus, glossopharyngeal, and facial nerves were originally provided with ventral roots in addition to their dorsal and lateral ones, and that probably the abducens was diverted to its present disconnected position by the migration of the more ventral pre-otic musculature to the vicinity of the eyeball. The recurrent branches of the abducens should be correlated either with the migration forward of a postotic myotome to form the external rectus muscle, or, as Neal suggests, with the loss of the postotic myotome and the ‘piracy’ of the nerve in acquiring attachment to pre-otic muscles.

If we examine the descriptions and drawings of those authors who have mentioned these recurrent branches, mostly in connection with studies on the derivation of the eye muscles, the impression is left that they are occasional variations, small and of significance only in the comparative morphology of the vertebrate head. Neal} describing Acanthias, says “that not all of the nerve fibrils extend anteriorly toward the third sornite (van Wijhe’s), but that in later stages of development, e.g., in embryos with 70-80 somites, a nerve fibril is seen to pass from the posterior root of the nerve in a posterior direction toward the inyotome of the sixth somite.” Miss P1att2 speaks very briefly of the abducens, also in Acanthias, as being “at first distributed not only to the Walls of the third head cavity, but also to the general mesoderm posterior to that cavity.” Thus two investigators find these recurrent branches in the same class of vertebrates at different embryonic ages, the one ‘at first,’ the other ‘in later stages.’ Scammon, in the N ormentafeln of Acanthias, does not mention these branches, and in the material used by Scarnmon in this laboratory, I have found them in only one or two embryos, and then only as two or three short nerve fibers, soon lost and with no connection with the muscle.

‘Flatt, 1891.2, p. 171.. {Full data for references in foot notes are given in bibliography.) 2 Neal, 1898, p. 232.

Dohrn[1] in an early paper describes the abducens inTorpedo: “it is further noteworthy that the root fibers at their first appearance are directed analwards, like the motor spinal nerves, and that only after a certain course in this direction the separate root bundles run together into a common nerve stem, directed forward.” This is obviously not meant to imply a recurrent branch of the abducens in the strict sense; but later Dohrn4 did find such branches in Heptanchus cinereus. On the left side of an embryo of 23 mm. he observed and drew carefully a large branch running dorsalward and connecting with the myotome called by him ‘u.’ He apparently did not know of Miss Platt’s work, and only later of Neal’s, to which he refers in a foot-note. The branch was represented on the right side by a much smaller nerve, reaching only half as far. He considered it so little likely that such a picture should be pure chance, that it became of great importance to search in the other embryos to see whether in them also a ramus recurrens of the abducens could be found, and in fact succeeded in finding it in a 14-min. embryo on both sides, though in a much reduced form, as a short wavy nerve of only one fiber; and in an embryo of 20 mm. on the left side only, also as a short branch. Thus after careful search he found it in three out of some dozen Heptanchus embryos studied, and in all but one case “in a much reduced form.”

Belogolowyfi studying the cranial nerves of the chick, finds frequently three groups of rootlets for the abducens, the first pointing forward, the second indifferent, and the third pointing mostly backward; they become, as his figures show, connected with each other and with the most anterior hypoglossal roots by slender bundles of fibers, making a continuous nerve parallel with the floor of the medulla and prolonging the abducens caudally to the hypoglossal nerve. This arrangement is found in chicks of between three and five days’ incubation, and is terminated by the loss of the ventral roots between the two definitive nerves, so that the nerve origins become separated by a widening gap. None of these transient rootlets or connections grows toward the vagus or glossopharyngeal nerves, and there is no evidence that any fibers have an independent growth caudally from the permanent abducens roots. Belogolowy examined also pig embryos for comparison of the head nerves with those of chicks, and figures in an embryo of 3 mm. frontoparietal measurement (about 8 to 9 mm. greatest length) short rootlets continuing the ventral series between the abducens and hypoglossal, but without joining either of these nerves. These I have also found in the majority of the 125 class specimens of 10- to 12—mm. pig embryos cut in transverse section (though in this plane they are not conspicuous) and in some of the younger specimens in the collection. None of these is of more than a few fibers, and, as Belogolowy noticed, none remains for longer than the growth period of 5 or 6 mm.

In sheep and rabbit I find even these rootlets much less frequently, so that a recurrent branch of the abducens must be very rare in these embryos. In many of the rabbit embryos of thirteen or fourteen days the anterior XII roots run between the vagus and the glossopharyngeal nerves, but these seem to disappear wholly after this time. They have no connection with the abducens, all of whose fibers point immediately forward.

In Lacerta muralis, between 5 and 7 mm. in length, and in Chrysemys marginata, from 7 to 9 mm., the abducens is provided with a few posterior rootlets, joined in loops, behind the permanent roots. In this respect these two species of reptile resemble the birds (chick), but the rootlets do not extend as far caudally in the reptiles, and there is never, apparently, a continuous connection between the abducens and the hypoglossal. I have found no remains of these rootlets in older embryos.

From this brief resume of the findings in Acanthias, Heptan— chus, chick, reptile, pig, sheep, and rabbit, it is clear that transient nerve roots arising from the ventral surface of the hind brain between the permanent abducens and hypoglossal roots are to be expected in a certain, usually small, percentage of these embryos. They are commonly small enough to escape notice unless under special scrutiny. In man they are more constant, larger, and apparently of longer duration (found in relatively older embryos) than in any other of these groups.

Of the twenty—four human embryos in this collection between the first appearance of the abducens nerve and the crown—rump length of 18 mm. only two are entirely lacking in this respect; three others have the recurrent branch on one side only. The two embryos of this group, one of 12 mm. (H. E. C., no. 816), the other of 16 mm. (H. E. C., no. 1128), which lack the recurrent branch, show instead long anterior hypoglossal roots running in front of the vagus nerve, between it and the glossopharyngeal. Between 18 mm. and 31 mm. there are again twenty—four embryos, of which twelve are provided with the recurrent branch on one or both sides. Beyond this age I have not found it present. As there is evidence that these branches may degenerate and disappear as early as the 15-min. stage, the first group of tWenty—four embryos would seem to be a fairer index of the usual occurrence of this feature, and one might state therefore that the recurrent branch of the abducens is present in over 90 per cent of human embryos; in other words, that their absence is an anomaly, their presence, up to the 18—mm. stage, to be normally expected. .

In spite of this fact, these branches have been noticed only three times, to my knowledge, in papers on the description of individual human embryos. Phisalix, in 1887, writing of the cranial nerves of a human embryo of thirty—two days, 10 mm., seeks to prove that the cranial nerves are similar to the spinal, and after mentioningthe dorsal and lateral roots of the vagus and glossopharyngeal nerves contin.ues:“ “Beside these intrabulbar motor roots I have discovered others which (litter in no way from the anterior spinal roots, neither in their origin nor in their connections. Thus for each of these nerves there is a very slender bundle of motor fibers which arises from the bulb, at its base near the median line, a11d which runs to join the nerve at the distal end of the superior ganglion.” No drawing accompanies this description, but it is evident that either anterior hypoglossal or posterior abducens roots are indicated. Thyng[2] speaks of the presence in a 17.8-mm. embryo of a caudal aberrant root on each side running from the region of the vagus and glossepharyngeal nerves to join the abducens. This embryo is in this laboratory, and represents one of the better examples of recurrent branches—the root to the abducens being actually a branch from this nerve, ending below the upper ganglion of the vagus. Barnivilles describes a posterior root or branch of the abducens in a human embryo of 8.5 mm., Which, joining a branch from the most anterior hypoglossal nerve, turns dorsally, like a dorsal ramus of one of the spinal nerves, and extends to the level of the ganglionic commissure of the vagus, where it comes very close to the brain wall. Barniville is in doubt whether it actually has a connection here or not, and therefore in doubt whether to call the fibers sensory roots of the hypoglossal and abducens, or dorsal rami of these nerves. He refers to my earlier figures, where similar dorsal rami are shown. Streeter, in his article on the cranial nerves in the Keibel-Mall Textbook of Embryology, mentions the aberrant roots of the abducens and hypoglossal nerves as possible results of a caudal extension of the abducens nucleus or cephalic extension of the hypoglossal nucleus, but gives no hint of their frequency, and does not mention or figure the recurrent branches. Elze, in 1907, describes two roots of the abducens in an embryo of 7 mm., one arising far caudally; but this is not a recurrent branch, as the posterior fibers pass forward from the brain to join the anterior root on the way to the eye muscles.

° Phisalix, 1887.2, p. 243.

Several reasons may be considered for‘ the failure of other investigators to notice these recurrentbranches of the abducens in man: the usually transverse plane of section places the abducens roots at a disadvantage, cutting them across where they are smallest at their origin from the medulla floor and where small branches of the vessels entering the medulla are very numerous and in close relationship with the nerve roots, thus making their presence difficult to detect; in fact, the roots may run in the walls of these vessels for a considerable distance. The not uncommon shrinkage of the brain in preservation may break the small abducens roots and make their connections uncertain. Another consideration is that in the usual reconstruction of the cranial nerves as seen from the side the abducens is partially hidden by the large ganglion of the trigeminal and by the otocyst and its attendant ganglia, and therefore perhaps not so much an object of study as the other nerves. Finally, it may be possible that the human embryos of this collection are too few to justify any statements as to the frequency of the presence of these recurrent branches, and that with a wider study a much smaller percentage would be obtained.

Considerable variation in the exact origin and course of the recurrent branches is found, but it is possible to designate certain types into which all may be grouped. In their method of origin from the medulla floor they may arise with the main abducens roots, some of the fibers from the same roots pointing caudally, some curving sharply forward, so that there is a crossing of the individual bundles in the same roots; or the recurrent nerves may arise by one or more separate roots, closely caudal to the last abducens root. The usual course is ventral and lateral toward the jugular foramen, with the vagus and glossopharyngeal nerves, but some pass laterally, to the dorsal musculature of the neck, while others turn dorsally, as in the cases described by BarmVille and by me formerly, to end beside the more dorsal part of the hind brain. It is quite common to find the recurrent branch doubled on one or both sides of an embryo, as in figure 1, and, as is shown there, the two branches may be joined at some distance from the brain wall. In size there is again great variation; some recurrent nerves are of a few fibers only, others as large or larger than the abducens itself; frequently the large branches end in terminal expansions. In length they also vary, some running only a few micra, others extending past the vagus nerve far ventrally or far laterally to the musculature, as has been noted.

The fate of these recurrent branches is undoubtedly degeneration and complete disappearance, as no record has ever been made, to my knowledge, of their presence after the .31-mm. stage. The course of this degeneration can be followed in my specimens with a fair degree of certainty. At first the nerve fibers of the branch, especially at their tips, become wavy and slightly separated from one another, thus causing the terminal expansion mentioned above. Then follows a reduction in the number of fibers in the proximal portion of the branch, near the nerve roots. All gradations of this peculiar feature can be seen in different embryos, from a scarcely noticeable change of size in the two ends of the branch to a complete severance of the distal end from its origin, so that the nerve fibers, still readily recognizable, lie in the mesenchyma entirely separated from the medulla and from the main abducens nerve. Whether or not this is preceded by the degeneration of the nerve ‘cells in the abducens nucleus, I have no means of judging, as the material available is not stained to show the details of nerve-cell degeneration. No obvious differences in the cells of the nucleus are noticeable in any of the specimens. Similar free fibers have been noticed and figured before by me and by T-hyng9 in relation to the degenerating anterior hypoglossal roots, but the result was not so striking in that case, as the nerve bundles were distally connected, at least physically, with a live nerve; the degenerating branches of the abducens nerve, with no connection at either end, seem much more surprising. The final dissolution or absorption of the disconnected nerve fibers is apparently accomplished by the action of phagocytes. The process, as shown in figure 4, is indicated by the presence within the nerve bundle of phagocytic cells in various stages of engorgernent, as evidenced by vacuoles in the cell protoplasm; they are apparently recruited from the surrounding mesenchyma, and pass out into it again after engorgement, or perhaps they are cells of the perineurium in a new role. The cell reaction is slight, as only a few small phagocytes are ever found, showing that the process is slow and gradual; but these few cells are easily recognized, as they are the only cells among the nerve fibers which throughout the abducens are _free from nuclei, except for the perineurium. The end result is the total disappearance of the recurrent branch. In one embryo I have seen a small group of phagocytes, present in only three consecutive sections, clustered about two or three scarcely recognizable nerve fibers. Only its position, along the usual course of the recurrent branch, made me reasonably certain that this group of cells represented the last stage in the process of dissolution of this nerve.

° Sec figure 1, at, and also Bremer, 1908, figures 1 and 2, cc. Thyng, 1914, plate 3.

Diagram A The floor of the medulla is seen in profile from the right side, with the proximal ends of the glossopharyngeal, vagus, and hypoglossal nerves. The main abducens points to the right, the recurrent branch to the left‘. In nos. 1, 2, and 3 the different courses of the recurrent branches are shown‘, to the occipital somitic muscles, to the branchial muscles, accompanying either the vague or glossopharyngeal nerves, and to the postotic dorsal musculature, respectively. N0. 4 gives a variation showing a separate root for the recurrent branch. No. 5 shows a degenerating recurrent branch so short that its destination is not certain, and already disconnected from its nucleus in the medulla.

Usually the recurrent branches either degenerate relatively early, before the precartilage of the base of the skull is laid down, or if they persist pass toward or through the jugular foramen with the vagus and glossopharyngeal nerves. On the left side, however, of one embryo of 25 mm. (H. E. C., no. 2042) the long Well-marked recurrent branch, larger than the main abducens nerve, passes through a separate foramen, Walled off from the jugular foramen by a substantial plate of precartilage, and containing in addition to the recurrent branch of the abducens a meningeal branch from the trunk of the vagus, and a small vein, probably the inferior petrosal sinus. These two structures commonly accompany long recurrent branches of this type, but the partition of precartilage across the jugular forarnen I have seen in no other embryo. It probably marks off the anterior compartment of the jugular foramen mentioned in some textbooks of anatomy as containing the inferior petrosal sinus, but in other embryos of this age, and even considerably older, the cartilaginous plate does not exist, nor is it present on the right side of this embryo, where the recurrent branch is much shorter. The possibility is strongly suggested that this early subdivision of the jugular foramen is caused by the presence of the recurrent branch, and a bony canal in this position might even be looked for as an anomaly. In attempting to explain the fact that the recurrent branches of the abducens nerve attain in man their greatest duration and size and frequency, obviously phylogenetic considerations are of no assistance. Nor can We turn with any hope of enlightenment to the history of the head somites, for they are not recognized generally in man, in spite of a paper by Zimmerman, who reported finding them in an embryo of 3.5 mm. VVe are forced to an examination of the nerves themselves at their earlier stages, and of any adjacent structures which might influence them, in the search for a possible explanation.

The earliest abducens root fibers in man leave the medulla wall at right angles to its surface, and continue growing in this direction for a considerable distance. In an embryo of 7.5 mm. (H. E. C., no. 256) and in another of 9.6 mm. (H. E. C., no. 1001) the fibers point straight away from the brain wall. In one of 6 mm. (H. E. C., no. 2094) the very few fibers as yet present curve slightly at their distal ends, and point some cranially, some caudally, in about equal numbers. In an embryo of 4.6 mm. (H. E. C., no. 374) a single rootlet divides, sending a recurrent branch caudally and the main nerve cranially, both short, but of about equal size and length. Another rootlet is just emerging from the brain on one side a short distance cranially. Incidentally it will be noted that the total length of these embryos is not a reliable measure of their development at this time, the smallest of this group being really the oldest in general configuration as well as in the growth of the abducens nerve. The first rootlet, then, seems to be attracted both forward and backward with equal force, and the individual fibers seem to hesitate, and often interdigitate in their final course. I have already noted that Dohrn found these rootlets in a similar condition in Torpedo, but after a short caudal growth they usually all turned forward. In pig, sheep, and rabbit, on the other hand, the first abducens roots turn cranially almost from the start. Apparently, then, there is in man some force acting on the earliest growing fibers to turn some of them caudally, a force which is lacking or of insufficient strength at the crucial moment in other mammals.

Another point to be taken into consideration is the relative time of the emergence of the numerous abducens rootlets. Belogolowym makes the observation that in chicks the anterior spinal nerves appear earliest, and the motor nerves of the brain later, but that the order of development of this forward group is subject to great variation. Of the abducens roots particularly he makes this generalization,“ that in birds they develop one after the other from behind forward, while in mammals the reverse is true, the growth of the abducens rootlets spreading backward toward the hypoglossal nerve. This generalization is, I think, too broad, and was probably made after the study of only the two classes of embryo mentioned in his paper, namely, the chick and the pig. It also might properly be amended to include the other ventral cranial nerve, the oculomotor, arising still farther forward. With this in view, I have examined embryos of sheep, pig, and rabbit, and find in each that, as Belogolowy states, the abducens roots emerge serially from before backward, and that in each the development of the oculomotor nerve precedes that of the abducens. In man, on the other hand, if one may judge by the four embryos available at this critical stage, the abducens is the earlier of the two nerves, and the growth wave spreads forward. The oculomotor nerve seems to grow much faster and reaches the eye muscles sooner than the abducens, which would lead to a false idea of their relative priority. Thus the first rootlets of the abducens are probably the caudal ones, nearer and therefore more suceptible to any postotic attraction; while in the other mammals studied the earliest rootlets are cranial and therefore removed from this attraction and brought nearer to a pre—otic influence. Both influences act apparently even as far back as the first human roots, vying with each other and causing the divergence of the individual fibers.

W Belogolowy, 1910, p. 270. 1‘ Belogolowy, 1910, p. 322.

The attractions suggested are, of course, the masses of developing muscle, the pre—otic eye muscles rapidly developing, and the postotic premuscle mass either degenerating or migrating forward, according to the two prevalent theories of 'the loss of the postotic myotome. In the human embryo of 6 mm. mentioned above, in which the abducens fibers are short and turn, some cranially, some caudally, and in which the oculomotor nerve is as yet absent, the occipital muscles are already indicated by a continuous band of elongated cells in the somites extending as far forward as the vagus ganglion. Ventrolateral to this ganglion and again ventrolateral to the glossopharyngeal, facial and trigeminal ganglia, there are condensations of mesenchyma, but without elongated cells. After a gap there is again a mesenchymal condensation dorsal and caudal to the eye, in which elongated cells are found. In the 9.6-mm. and 7.5—mm. embryos of about the same age, the eye—muscle mass is not so clearly defined, but the sornitic muscle is continuous up to a point just caudal to the vagus ganglion. In a sheep embryo of 7.2 mm. (H. E. C., no. 1226), on the other hand, the oculomotor nerve is large and can be traced to a well-defined eye—muscle mass, while the somitic muscle ends some distance caudal to the vagus; the abducens is just beginning, and turns almost immediately forward. The same is true in rabbit embryos of 5 mm. (twelve days), as regards the oculomotor and abducens nerves and the disposition and condition of the muscle masses. A difference exists, however, between sheep and rabbit in the extent of the hypoglossal roots, which are confined to a caudal position in sheep, but reach far forward in rabbit, in these early stages, leaving only a small gap between them and the abducens roots‘. The corollary of this appears in the frequent occurrence in the latter embryos of anterior hypoglossal roots passing in front of the vagus nerve. In the rabbit the earliest roots of the abducens are almost pre-otic and actually nearer to the eye-muscle mass than to the isomitic muscle. In the pig the muscles have about the same disposition as in man, but the oculomotor nerve arises first and the eye—Inuscle mass may be considered to predominate and attract the anterior abducens roots, which arise next in order ; the later, more posterior abducens roots, however, point frequently toward the occipital muscles, to which they are nearest, giving the small short-lived recurrent branches, which are always separate roots, not interlaced with those of the abducens proper.

In the chick the order of emergence of the abducens rootlets seems to progress usually from behind ‘forward, as Belogolowy said, and they are at first a continuation of the anterior hypoglossal roots. This would lead one to expect recurrent branches, as the order is similar to that found in man, as opposed to sheep and rabbit. The oculomotor nerve is, however, Well developed before the abducens appears, probably in conjunction with the large and precocious eye, which is accompanied by precocious eye muscles. The external rectus is already recognizable as a separate muscle in chicks of little over forty—eight hours’ incubation, and in an embryo of about three days, 6.2 mm. (H. E. C., no. 511), is well developed and with clear—cut edges, though the abducens fibers have not yet emerged from the brain. The large eye has also altered the position of this muscle, the caudal end of which lies far caudal to the anterior edge of the trigeminal ganglion, much nearer the otocyst than in mammals. The occipital muscles in this embryo are also readily recognizable, and end with a sharp edge medial to the vagus ganglion. The abducens roots, as they emerge, would perhaps feel the attraction of both muscles, the anterior group of them turning forward, the posterior group backward, and the intermediate group indifferent, as described by Belogolowy. These groups, however, include all the rootlets back to the hypoglossal nerve, Whereas the anterior alone remain permanently as the abducens nerve, and since these have been influenced by the proximity of the external rectus muscle, no recurrent branches in a strict sense are found. Belogolowy figures fibers continuing the abducens caudally, to be sure, but a study of their course and shape shows that they are the remains of more caudal rootlets which were attracted forward to join the abducens by loops, and which now are degenerating, by loss of their connection with the brain, as in the case of the degenerating hypoglossal roots already referred to. In other words, they are the remains of cranially directed fibers from caudal rootlets not caudally directed recurrent fibers.

The disposition of nerve roots and muscle masses in Lacerta and Chrysemys is similar to that just described in chicks. The permanent, cranial abducens rootlets are much nearer to the large, external rectus muscle than to even the most cranial of the occipital muscles, and the caudally disposed abducens rootlets degenerate so rapidly that no recurrent branch becomes established.

In Acanthias new elements seem to influence the course of the abducens fibers. The lack of a neck bend would remove the occipital muscles relatively farther caudally, but the more complete development of the postotic head cavities would probably more than overbalance this; and the position of the nerve roots themselves tends further to approximate the postotic muscles and nerve roots. Belogolowy,” as noted by Neal, found that in Acanthias the roots of the abducens arise from neuromeres next posterior to those from which they originate in chicks, thus subjecting the caudal roots to a stronger postotic attraction, represented by the occasional recurrent branch. The same is very probably true in Heptanchus, but no material is available to me for examination. The presence or absence of a recurrent branch would depend upon a delicate balance between the time of emergence of the fibers from the brain and the degeneration of the postotic somite, or perhaps its ability to produce muscle fibers.

It will be seen, then, that the presence of recurrent branches of the abducens is correlated with the proximity of postotic premuscle masses to the emerging roots, supplying apparently an attraction in opposition to that of the eye-muscle group. Probably the degree of differentiation of the various muscles concerned plays a large role in the force of these attractions, independent of their actual proximity, but our lack of knowledge of the minute details of early muscle differentiation, or of possible difference between muscles developed from definite somites and those, like the eye muscles and the branchial musculature, arising from Inesenchymal condensations, does not permit us to be critical in this respect. The three types of distribution of the recurrent branches, to the lateral head musculature, to the branchial muscles accompanying the vagus nerve, and to the dorsal side of the head, show further that the postotic influence may be from different sources. The first two types have a common course as far as the line of the Vagus and hypoglossal junction, and the majority of recurrent branches follow this course, but end before reaching the vagus, so that it is impossible to tell whether they would have continued laterally or curved to accompany the vagus or hypoglossal nerves. In the first case the muscle attraction Would have been the most anterior somite, in the latter the mesodermal condensation to form the branchial muscles. The third type represents those recurrent branches which turn dorsally, along the wall of the hind brain. Here we must suppose, if the musculature plays any part in determining their course, that certain cells of the somites migrate dorsally, as in the body somites, attracting the nerve fibers with them as dorsal rami. The same possibility is invoked by Neal and others to explain the course of the trochlear nerve, and it may be of interest to record that in one embryo of 16 mm. (H. E. C., no. 2095) the trochlear itself, though otherwise normal, has dorsal rami in the form of short branches which pass dorsally from each nerve just lateral to the chiasma. The lateral muscles have retained their position, the ventral or branchial and the dorsal muscles have migrated, carrying their nerve branches with them.

12 Belogolowy, 1910, p, 279.

In connection with this discussion of the probable causes of the development of the recurrent branches of the abducens, it is of interest to describe a human embryo of 18 mm. which shows a total absence of this nerve to the external rectus muscle. The embryo, which was cut in the sagittal plane, was found too poorly preserved for the regular Embryological Collection, and so kept in a supplementary group, and numbered 393. In spite of the poor preservation, however, all nerves can be readily followed, and such structures as muscles and organs easily recognized; the brain and allied structures have, as usual, suffered the most damage.

Complete absence of the abducens nerve on one or both sides is recorded as a rare anomaly in text—books of anatomy, but I know of no mention of its occurrence in embryonic stages. The external rectus muscle is in these cases usually supplied by a branch from the oculomotor nerve, and that is true in this instance. No other anomalies, except those noted in connection with this nerve, were found on casual examination.

On the left side the abducens is entirely absent; no trace of fibers arising from the medulla in the usual ventral position can be found between the roots of the oculomotor and those of the hypoglossal nerve. A peculiarity in the lateral nerve roots is the presence of a fairly large bundle which emerges between and in line withithe lateral roots of the trigeminal and facial nerves and runs medially and ventrally to join the tympanic branch from the petrosal ganglion of the glossopharyngeal nerve, median to the gasserian ganglion, to form with it the small superficial petrosal nerve. It is to be considered, therefore, merely as the motor facial component to this nerve, which arises more cranially than usual and takes a separate course, at a considerable distance from the genieulate ganglion. It passes through a separate foramen in the precartilage of the base of the scull.

On the right side of this embryo there is again no forwardrunning abducens nerve; the external rectus muscle is supplied by a branch of the oculomotor. But in the usual position of the abducens roots fibers arise which turn ventrally, slightly caudally, and laterally to join the motor division of the facial nerve, distal to the geniculate ganglion. Thus a ventral root from a position slightly cranial unites with a lateral root just beyond the ganglion of the accompanying dorsal fibers, and the relations of a complete nerve are closely approximated.

Applying to this case the ideas gathered from the study of the recurrent branches of the abducens, I examined the eye muscles of this embryo, and also the various parts of the eye itself. The external rectus muscle was clearly differentiated on both sides, the eyes were apparently normal, though the retina and lens were in a poor state of preservation. But in comparison with other embryos of the same size and even smaller, it Was found that the eye and all its appurtenances were definitely retarded. The retina was thinner and less differentiated, the lens showed shorter fibers and was still widely Vesicular, the eyelids were less developed and the "anterior chamber Was not even suggested, though already present in other embryos of 18 mm. As a Whole, the eye of this embryo resembled most closely that of a 14.5 mm. embryo. With this retardation of the eyeball, the eye muscles Were found to be much smaller than usual, though clearly differentiated.

The probable history of the abducens nerves in this embryo can, then, be sketched as follows: all of the emerging fibers were submitted to the caudal attraction of the postotic musculature or of the branchial muscles, and, because of the probable late development of the eye and its accompanying structures, were relieved from the usual counter-attraction of the eye muscles. Even the most anterior rootlets thus turned caudally, not, to be sure, to the occipital muscles, but to the ventral condensation for tl1e muscles supplied by the facial nerve. A little later, after the abducens fibers had all emerged and taken a caudal course, the eye muscles developed and attracted the oculomotor nerve, Which, since the external rectus muscle was unprovided by its usual nerve, sent an unusual branch to this muscle also. Of the recurrent branches of the abducens we can imagine that only the most anterior on one side has persisted, all the others undergoing the degeneration commonly found before this age. Probably the one remaining would soon have disappeared; in fact, its caliber at its origin is already much less than at its union with the facial nerve, and in the brain the nucleus of the abducens, apparently entirely absent on the opposite side, is very doubtfully represented by a slight grouping of cells.

It seems probable, then, that the absence of the abducens nerve in a human subject is due to some very unusual retardation of the development of the eye, which causes the abducens fibers, released at the crucial moment from any anterior attraction, to tur11 caudally, thus leaving the external rectus muscle free to be annexed by some other nerve. With the degeneration of the recurrent abducens fibers, as is always to be expected, the nerve in these cases is completely lost, an.d no trace of its original emergence from the brain is carried into adult life.


Recurrent branches of the abducens nerve consist of fibers whose growth is in a caudal or ventrocaudal or dorsocaudal direction. They are present infrequently in Acanthias, Heptanchus, and pig, absent in chick, lizard, sheep, and rabbit.

They are most frequent in man, Where they appear in about 90 per cent of embryos up to 18 mm., and less frequently up to 31 mm., since they may begin to degenerate at 15 mm. Degeneration is shown by the separation of the fibers from the brain (probably after loss of the nerve cells in the abducens nucleus) and their digestion by phagocytes.

The distribution, of those fibers long enough to make their destination sure, is to the anterior spinal muscles, the branchial musculature, or the dorsal muscles of the head. They may arise from the same roots as the abducens proper, or by separate but closely adjacent rootlets. They are absent in embryos whose eye muscles predominate over the occipital muscles, either by proximity or precocity, but the position of the first abducens roots on the floor of the medulla is also a factor, as the more caudally these arise, the more often are recurrent branches to be expected. Among the mammals studied, man alone shows the abducens roots emerging in order from behind forward, with the oculomotor appearing later than the abducens. In sheep, pig, and rabbit the growth wave is reversed, beginning with the oculomotor and extending caudally.

In man, then, the earliest abducens roots are caudal, nearer to the occipital muscles, in the other mammals they are cranial, approaching the eye-muscle mass. In birds and reptiles the eye and its muscles are not only precocious, but the muscles are actually displaced caudally by the large eyeball, so that their influence on the emerging abducens fibers extends far caudally and only the fibers close to the hypoglossal roots turn caudally. These are soon lost, and the permanent abducens shows no recurrent branches. In fishes the abducens roots arise from more caudal neuromeres, and occasionally some fibers turn caudally, but only as a rare anomaly.

Literature Cited

Barniville HL. The morphology and histology of a human embryo of 8.5 mm. (1914) J Anat. Physiol. 49(1):1-71. PMID 17233012

BELOGOLOWY, J. 1910 Zur Entwickelung der Kopfnerven bci Viigel. Bull. Soc. Imp. Moscou, Hft. 3, 4.

BREMER, J. L. 1908 Aberrant roots and branches of the abducent and hypoglossal nerves. Jour. Comp. Neur., vol. 18, no. 6.

DOHRN A. 1890.2 Studien u. s. w. 15, Mitt. Zool. Stat. Ne-ape], Bd. 9. 1901 Studien u. s. w. 18-21, Mitt. Zool. Stat. Neapel, Bd. 15.

ELZE, C. 1907 Beschreibung eines menschlichen Embryo von zirca 7 mm. Anat. Heftc, Heft 106.

NEAL, H. V. 1898 The segmentation of the nervous system in Squalus twanthias. Bull. Mus. Comp. Zool. Harvard, vol. 31, no. 7.

1914 The morphology of the eye muscle nerves. Jour. Morph, vol. 25, no. 1.

PLAT1‘, J. B. 1891 Morphology of the vertebrate head. Jonr. J. Morph., vol. 5 no. 1. '

PHISALIX, C. 1887 Sur les nerfs cranien d’un embryo humain de trente-deux jours. Comp. rend. acad. sc. Paris, T. 104, ‘no. 4.


SCAMMON, R. E. 1911 Normal plates on the development of Squalus aeanthias (F. Keibel).

Streeter GL. The Development of the Nervous System. (1912) chapter 14, vol. 2, in Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia.

Thyng FW. The anatomy of a 17.8 mm human embryo. (1914) Amer. J Anat. 17: 31-112.


Plate 1

1 Human embryo of 16 mm. (H. F. C., no. 2095). Median View of the left side of the caudal half of the medulla oblongata, showing the first cervical and hypoglossal nerves, and beyond them the accessory and vague complex and the g1ossopharyng;ea.l nerve. The lower ganglia of the vagus and g1ossopharyngeal nerves are fused, and crossed in the drawing by two sympathetic branches. The abducens shows the main nerve double, the two parts meeting just beyond the limit of the drawing, and two recurrent branches joined by a slender strand, the larger of which points toward the sympathetic nerves. The roots indicate that some fibers arising caudally pass to the main nerve, and some of those quite far forward run caudally to the recurrent branches; but the most cranial roots all point forward. At ‘ac’ is a degenerating anterior hypoglossal root, disconnectcd from the medulla. 393

Plate 2

2 and 3 Photographs of sections 347 and 368 of the embryo shown in figure 1. The plane of section is transverse, nearly parallel to the upper recurrent branch. The median line is marked by the bzxsilar artery, at the left, below which is seen the edge of the medulla. Behind the thick-walled otocyst the glossopharyngeal, vagus, accessory, and hypoglossal nerves are shown in cr0ss—sec~ tion. Figure 3 cuts the upper recurrent branch as it turns laterally to enter the jugular foramen; figure ‘2 shows the lower recurrent branch lying in the floor of the same foramen, and, between it and the medulla, the scattered rootlets of the main abdueens nerve are seen. X (35.

Plate 3

4 Detail under high power of the tip of the lower recurrent branch of the abdueens shown in figure 1. The nerve fibers, surrounded by a perineurium, have been invaded by;ocytos, which become vacuolated and apparently cause the dissolution of the fibers, as evidenced by the vacant spaces within the nerve sheath. Some of the engorged phagocytes can be seen among the cells of the perineuriurn. (H. E. 0., no. 2095, sect. 269.) X 600.

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  1. Dohrn, 18902, p. 343. 4 Dohrn, 1901, p. 28. 5 Belogolowy, 1910, p. 271.
  2. Thyng, 1914, p. 56. 5 Barniville, 1914. p. 11.