Paper - The development of the cranial nerves of vertebrates 1 (1891)

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von Kupffer C. The development of the cranial nerves of vertebrates. (1891) Translated by Oliver S. Strong J Comp. Neurol. 1: 246.

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The Development of the Cranial Nerves of Vertebrates

Professor C. von Kupffer.

  • Report read at the meeting of the Anatomical Society at its fifth annual session, at Munich, May i8, i8qi. Translated for this journal, from advance sheets, by Oliver S. Strong, Fellow in Biology in Columbia University.

Gentlemen :

There is scarcely need of the assurance that I do not stand before you with the pretense of presenting the comprehensive subject of my report with perfect sj'mmetry on all sides. Tliat would only be possible if the development of the vertebrate head as a whole could receive thorough treatment at the same time. The works which relate to the cranial nerves are still issuing, and it is difficult to predict, up to the present, how the course of these works will influence the solution of the problem of the vertebrate head.

In consideration of the time here allotted to such a report, I limit my remarks to a condensed summary of the present trend and results of research in relation solely to the morphogeny of the cranial nerves, apart from their histogeny and from the remaining phases of the problem of the head.

So much may be said in advance: that in the formation of the vertebrate head very remarkable reductions and fusions of endodermal and mesodermal parts, and, in connection therewith, of the peripheral nervous system, extending in direction from before backwards, have occurred. And, further, I venture to assert that, besides a branchial system of cranial nerves, sharply distinguishable genetically from the spinal system and belonging to the gill apparatus, a spinal system of dorsal nerves has likewise more or less completely maintained itself.

The old theory of the spinal nature of the cranial nerves, dating its beginnings from Proschaska and Sommering, received weighty support through the Goethe-Oken vertebrate theory of the skull; it outlasted the latter doctrine, and appeared until recently consistent with Bell's law. But the embryological works of the last decade have so severely shaken the foundations of this doctrine that so decided a defender of it as C. Gegenbaur(') found himself obliged to admit that the homodynamy of the cranial and spinal nerves appeared to him no longer tenable. The first shock this theory received was through the observation of Balfour,( ') on elasmobranch embryos, that the mixed cranial nerves are decidedly of dorsal origin, and they are also to be distinguished essentially from the dorsal roots of spinal nerves owing to the motor elements in them.

While Balfour did not succeed in finding in the region of the cranial nerves any roots whatever which might be compared with the ventral roots of the spinal nerves, he, on the other hand, did not doubt the complete validity of Bell's law, and accordingly advanced the hypothesis that there had existed originally a common fundamental form of the nerves in the whole body which are only represented by the dorsal roots of a mixed nature. At this stage the diflerentiation of head and trunk took place, so that the type of the spinal nerves corresponding to Bell's law would be regarded as secondarily acquired, while the cranial nerves have preserved the original condition. This hypothesis appeared to Balfour so much the more probable in that he decided, (') in opposition to the observations of Stieda() and Schneider, () that in Amphioxus ventral motor roots were lacking.

1 "The Metamerism of the Head and the Vertebrate Theory of the Cranial Skeleton," Morph. Jahrb , XIII, p. 64 and 104.

2 "The Development of the Elasmobranch Fishes," Journal Anat. and Phys.,Vol. XI, 1877, and Handbook of Comp Anat , trans, by Vetter, Jena, i88r, Bd. II, p. 411.

This hypothesis appeared untenable, since, on the one hand, ventral spinal nerves of a motor nature are found in Amphioxus, and, on the other hand, the development ot ventral nerves was observed in the region of the head, as, for example, the origin of the abducens from the ventral aspect of the medulla in the chick, as well as in Scyllium, by Marshall.

But, aside from the hypothesis, the fact remains that the undoubtedly dorsal cranial nerves do not conform to Bell's law, but are of a mixed nature.

Van Wihje's(^) treatise, appearing soon after the works of Balfour above mentioned, brougnt to light the new disclosures, known to you, concerning the ontogeny of the cranial nerves in Selachians as proof, on one side, that at least two pairs of muscle nerves in the head, the oculomotor and abducens, appear after the manner of the ventral spinal nerve roots, and, like these, innervate only muscles arising, as alleged, from somites, to which the eye-muscles should belong; while the motor elements of the cranial nerves arising dorsally are confined to the innervation of the muscles of the visceral arches, which proceed from the lateral plates. Relying upon this observation. Van Wihje impeached the validity of Bell's law, and showed the possibility that the relations discovered for the head have further application in the trunk, as in the enunciation of Bell's law the vegetative muscles in the t unk proceeding from the lateral plates were left out of consideration.

While Van Wihje sought in this way to establish the agreement between cranial and spinal nerves, he himself discovered at the same time facts w^hich cause the distinction between both groups to appear more marked than was hitherto supposed. On one side, he shows that the dorsal cranial nerves in respect to their course bear relations to the somites entirely different from the spinal nerves, and it furthermore emerges from his investigations that the epidermis participates in the development of the peripheral twigs of the cranial nerves, as G6tte(') and Semper(-') had already affirmed for the N. lateralis vagi.

1 " On tlie Spinal Nerves of Amphioxus," Quart. Jour. Mic. See, Jan., 1880, p. 90.

2 "Studies on Amphioxus Lanceolatus," Mem. d. I'Academ. d. Sc. de St. Petersbourg, 1873, I. 46.

3 " Contrib. to the Comp. Anat. and Devel. of Vert.," Berlin, 1878, p. 15.

4 " (Jn the Mesoderrasegments and the Development of the Nerves of the Selachian Head," Amsterdam, 1882.

Concerning the relation to the mesoderm, the dorsal cranial nerves first take their course over the mesoderm and on between the somites and the epidermis, but the dorsal roots of spinal nerves pass within and below the somites. This distinction is so important that it was especially by this that C. Gegenbaur was driven to abandon the homodynamy of cranial and spinal nerves, which he had previously defended.

According to Van Wihje's discovery, the facial, glossopharyngeus and vagus enter into close connection with the epidermis in a double row of points. On the one hand, fusion of their ventral branches occurs at the upper hinder side of the gill cleft which lies cephalad; on the other hand, the rudiments (Anlage) of their dorsal branches fuse with thickened portions of the epidermis. From the dorsal places of connection are developed portions of the lateral -line system with its nerves, in such a way that Van Wihje thought the participation of elements of the epidermis in the formation of the nerves might be regarded as certain. P'rom the places of fusion of the ventral branches with the epithelium of the gill clefts the terminal twigs of those branches are developed.

1 " Embryology of the Toad."

2 "Urogenital System of Plagiostomes," Arbeiten aus d. Zool.-Zoot. Institute zu Wurzburg, Rd. II, p. 398.

A. Froriep(') has pointed out the part played by the epidermis in the development of the cranial nerves in mammalian embryos, where, in comparison with the condition discovered by Van Wihje in Elasmobranchs, the share of the epidermis in this process seems scarcely less important. In cow embryos such processes take place in the region of the facial, glosso-pharyngeal and vagus, whose course is briefly as follows: In embrys 8-9 mm. long with three gill furrows apparent outside and four pharyngeal pouches, the spindleshaped ganglion of the facial unites with a pit-like, sunken and at the same time greatly thickened place in the epidermis, which corresponds to the dorsal extremity of the first external gill furrow. The same thing occurs with the glossopharyngeus; here also the distal end of the ganglion in the rudiment of this nerve unites with a greatly thickened and depressed portion of the epidermis dorsad to the second pharyngeal cleft. The vagus rudiment behaves similarly. Its large ganglion locates itself adjacent to a thickened epidermal surface, of the shape of a figure 8, which is situated dorsad to the third gill furrow and the vicinity of the fourth.

In cow embryos 15 mm. long the connections of the facial and glosso-pharyngeus are lost, but not of the vagus, and here the thickened mass of epidermis reaches deep into the ganglion, so that the two components cannot be definitely separated from each other.

Froriep compares these " organs of the gill clefts," though with reserve, to the connections, described by Van Wihje, of the ventral branches of the same nerves with the epidermis, dorsally to the gill clefts, and explains them as rudiments of sense organs which do not attain further development, and probably belong in the category of organs of the lateral line but with which they cannot be fully homologous, since the lateral organs of fishes are formed on the dorsal branches of the cranial nerves. As those ganglia which enter into the connections under discussion and accordingly originate through a union of central with epidermoid elements, Froriep indicates the gang, geniculi, gang, petrosum and gang, nodosum; they exhibit the phylogenetic remnants of former sense organs; they cannot consequently be considered homologous with the spinal ganglia, and thereby fails a chief support of the spinal hypothesis. The nerves of the visceral arches as segmental nerves can no longer be identified with spinal nerves.

1 " Rudiments af Sense-organs in the Facial, Glosso-pharyngeal and Vagus," Arch. f. Anat. u. Physiol., Anat. Abth., 1885.

In a long series of works J. Beard(') has handled the problem of the cranial nerves and their sensory end organs. Torpedo ocellata furnished the principal object of Beard's investigations, although sharks, teleosts. Amphibia and Amniota (Lacerta, chick) came under consideration. In the main. Beard follows, in facts as well as in the interpretation of the conditions, the observations and conceptions of the previously mentioned investigators, but also contributes the fact that the participation of the epidermis in the formation of ganglia and nerves occurs also in the region of the trigeminus.

The complete representation of the development of a dorsal cranial nerve would, according to him, be as follows: The rudiments of the ganglia in the head, agreeing throughout with those of the spinal nerves, arise as differentiations of the inner layer of the ectoderm, just outside the limits of the neural plate. They separate from the ectoderm, become displaced upwards in the closing of the neural tube, and come to lie between its lips, but are always distinguishable from it. After the closure of the neural tube, the portion of these rudiments corresponding to each cranial nerve grows ventrad, unites with the central organ by means of root fibres, probably growing out centripetally, and comes to lie on the outer side of the mesoderm, between this and the epidermis; while the rudiments of the spinal ganglia (of the trunk) proceed ventrally on the inner side of the mesoderm, thus between this and the central organ. These cranial ganglia rudiments, designated by Beard ^'■neuralganglia^ fuse at the level of the chorda with a thickened place in the epidermis dorsad of the neighboring gill cleft, which thickening represents externally the rudiment of a " branchial sense organ," internally that of a ganglion belonging to the latter, the '•'•lateral ganglion.' Here the elements of the neural and lateral ganglia blend indistinguishably with each other; there thus arises the definitive and apparently single ganglion of the cranial nerve in question. This separates from the epidermis — that is, from the rudiment of the branchial sense organ — but remains connected with the latter by a nerve strand, the suprabranchial nerve (dorsal branch of Van Wihje). From the ganglion are developed distally three nerves, namely, the JV. prcebrajtchialis , JV. postbranchialis , and \. pharyngezis. As to the N. suprabranchialis, it is, according to Beard, clear that it arises from the epidermis; for the N. praebranchialis he accepts the same mode of formation. With regard to the two other nerves, he remains undecided whether the epidermis takes part in their formation. (^) Beard regards it as certain in the case of the postbranchial twigs of the vagus(-) and in the case of the trigeminus (mandibularis).(')

I On the Segmental Sense Organs of the Lateral Line and on the Morphology of the \ertebrate Auditory Organ," Zool. Anz., 1884, p. 123; "The System of Branchial Sense Organs and their Associated Ganglia in Ichthyopsida," Quart. Jour. Mic:osc Sc, 1886. Vol. XXVI, new series, p. 95 ; '• The Ciliary or Motor-Oculi Gangl. and the Gangl. of the Ophthal. Profund. in Sharks," Anat. Anz., 1887, p. 585; " The Old Mouth and the New," Anat, Anz., 1888, p. 15 ; "A Contribution to the Morphology and Development of the Nervous Syst. of Verteb.," Anat. Anz., 1888, pp. 874, 899; "The Development of the Peripheral Nerv. Syst. of Vertebr ," Quart. Jour. Micros. Sc, Vol. XXIX, new series, 1889, p' 153; "Prof. Rabl on the Mode of Development of the \'ertebrale Peripheral Nervous System," Anat. Anz., 1890, p. 125.

For the trigeminus the same law of formation is said to obtain, inasmuch as the mouth represents a pair of gill clefts. But where gill clefts, with the musculature belonging, have entirely disappeared, yet sense organs persist, there, accord ing to this author, the structure is simplified; the N. postand

1 Quart. Jour. Mic. Sc, Vol. XXVI, 18S6, p. 102.

2 Ibidem, p. no.

3 Ibidem, p. 113.

prcebranchialis disappear, and the sole ones remaining are the N. suprabranchiales.

As such may be regarded: (i) The N. olfactorius (I segment), more clearly so after it was shown, through the olfactory buds discovered by Blaue, that the organ of smell belongs to the system of the lateral line, /.c, the branchial sense organs. 2. The ophthalmicus profundus (II segment), whose meso-cephalic ganglion (Gn. ciliare, Van Wihje, His) fuses with the epidermis close above and behind the eyes; later this root unites with that of the trigeminus, and the Gn. meso-cephalicum with the Gn. Gasseri.(') 3. The acusticus (VI segment), which is regarded as a remnant of a segmental nerve. The development of the nerve, of its ganglion, and of the ear, corresponds essentially to that of the homodynamous parts of complete segments. The auditory vesicle is the persistent, functionally modified branchial sense organ; the pertaining segment remains in the hyoid arch. Whether the aborted gill cleft is to be found, as Van Wihje thinks, behind the facial, or, as Dohrn takes it, is to be sought before the hyoid cleft, remains undecided.

Regarding the relation of cranial to spinal nerves. Beard at first declared himself in complete agreement with Froriep in so far as the dorsal roots and ganglia of the one could not be homologized with those of the other. Possibly Balfour was right, that the cranial nerves showed a more primitive condition than the spinal nerves, but it may be doubtful whether the spinal nerves ever had the same primitive character-(^) Later he changes this opinion, and, in regard to the supposed similar method of formation of the first ganglion rudiment in head and trunk, declares that there is a partial homology between the neural ganglia of the head and the spinal ganglia, but the first might possibly be only homologous with the sympathetic portions of the latter(*)

1 Anat. Anz., 1887, p. 565.

2 Quart. Jour. Mic. Sc, Vol. XXVI, 1886, p. 142-143.

3 Quart. Jour. Mic, Sc, Vol. XXIX, 1889, p. 153.

Judging from this, the entirely different position of the neural cranial ganglia on the one hand, of the spinal ganglia on the other, relative to the dorsal mesoderm, was not taken into account by Beard in the comparison.

In a lecently published article(') on the development of Petromyzon Planeri, I have likewise treated of the method of formation of the peripheral nervous system, in the course of which the previous works of Scott and Shipley on the same object received thorough consideration.

On the one hand, my observations not only yielded a confirmation of the participation, discovered in Gnathostomata, of the peripheral regions of the epidermis in the development of the cranial nerves, but caused this participation to appear still more considerable than could be admitted from what was previously known. But, on the other hand, facts emerged which do not accord with the results of the above mentioned authors, and display the complicated nature of the ci"anial nerves in a new light.

I was then led to essentially the following conception of the composition of the dorsal cranial nerves: Each one is composed of two parts, a spinal and a lateral., which latter, comprising all its components, can also be designated as branchial. The first behaves, with respect to its origin, its course and its relation to the dorsal mesoderm, entirely like a dorsal spinal nerve of the trunk. The dorsal cranial nerves thus originally contain parts homodynamous with the spinal nerves, but thereto is added the second variously formed component, which, arising with the spinal, proceeds over the dorsal border of the mesoderm and is situated on the outer side, between mesoderm and epidermis. It is these lateral components of the cranial nerves into whose composition growths of the epidermis enter, and that occurs in two series lying the one above the other. I distinguished them as lateral and epibranchial ganglia. The first lie in the horizontal plane of the auditory vesicle, and arise at three separate places, i.e., in the region of the trigeminus, acusticofacialis and vagus. The epibranchial ganglia likew^ise emerge descretely, and there is always one close above each gill pouch. The part of the corresponding cranial nerve proceeding over and outside the mesoderm secondarily unites with these structures, and, indeed, the union with the lateral ganglia is of such a nature that the rudiment of the nerve itself swells into a new ganglion, the medial (neural ganglion. Beard). From this union of the medial and lateral ganglia proceeds the definitive ganglion (Hauptganglion) of the cranial nerve concerned. The epibranchial ganglia take part in the development of the terminal twigs of the cranial nerves. In the separation of the lateral, as well as the epibranchial ganglia from the epidermis, there is nowhere shown the rudiment of a sense organ. With the sole exception of the auditory vesicle, which is formed in the closest proximity to the lateral ganglion of the acustico-facialis region and is homodynamous with this lateral ganglion, all these ganglia of both series are entirely independent structures, standing in no connection with principal sense organs.

X "The Development of I'etromy/on I'laneri," Arch. f. Mik. Anat., Kd. 35, 1890.

These were the results which I had reached. I had to break ofi' these investigations, on account of lack of material, at a stage in which the formation of the peripheral nervous system is far from concluded. It was the moment of the escape of the larvae (from the egg). I have since, with new and more complete material, carried the work on further, and extended it to the stage of larvae 4 mm. in length. At the same time I discovered that my older material, upon which the work cited had been based, contained gaps which prevented me from arriving at a complete understanding of the earliest beginnings of the cranial nerves. After interpolation of the then lacking stages of development, it is necessary to complete in many respects and partially correct my earlier representation.

The first rudiment I have sufficiently described and drawn. Towards the conclusion of the folding process taking place in the ectoderm, by means of which the massive central organ is formed, but before its separation from the ectoderm, one sees in the fore half of the embryo (head region) three cords, the median neural and the paired lateral cords, which latter, on either side, correspond entirely to the intermediate fascicles (Zwischenstrang) of His (Fig. i z).(') But I have not ascertained the succeeding phase since, as I now see, I have lacked the connecting links. I assumed that in the separation from the ectoderm the paired — /.e. , the intermediate — fascicles came at the same time to lie on both sides of the median neural cord, that is to say, of the massive brain. That is not the case; the paired rudiments move farther mesad together, so that they unite dorsad of the brain cord, into a plate lying between this and the epidermis (Fig. 2 d P), and which is distinguished from the regularly biserially arranged elongated epithelium-like cells of the brain by reason of the irregular and, subsequently, loose disposition of their elements. This plate exhibits the same structure which His had already sketched, in 1879, in a Scyllium embryo and Beard more recently has drawn in various elasmobranchs and of the chick.

Not to anticipate the difficult question as to which parts of the peripheral nervous system are derived from this plate, in our terminology I will refer to it neither as ganglionnor nerve-plate, but call it the dorsal brain-plate., since, although divided into three segments, it extends over the whole length of the brain. Furthermore, in the spinal cord I find the plate not so distinct and represented by a double row of cells, which my pupil. Dr. Victor Rohon, has first described, (■') albeit from later stages, in the trout.

1 Compare my drawings in the Arch. f. Mikr. Anat., 1890, Bd, 35, Taf. XXVIII, Fig. 25, and His' figure in the Arch. f. Anat. u. Phys., 1879, Anat. Abt., p. 465.

2 " On the Histiog. of the Spinal Cord of the Trout," Sitzgsber. d. math, physik. Kl. d. K. Bayer. Acad. d. W., Munchen, 1884, Heft I, p. 39.

Next the cells of the dorsal brain-plate advance laterad between brain and epidermis, forming the well-known ganglionor nerve-" border" (Leiste) of writers, and now it becomes necessary in considering the development of the cranial nerves to keep distinctly in mind the different regions.

I distinguish accordingly: ( i ) The region of the fore head to the eye, inclusive; (2) the fore gill region, comprising the mouth and the three fore gill pouches; (3) the hind gill region to the eighth gill pouch, inclusive; (4) the trunk region.

In the region of \k\.e. fore head (Fig. 3) begins the formation of the borders (Leiste), which I designate as rootborders ( Wurzelleiste), from the dorsal brain-plate, before the formation of the eye has begun; and the cells soon extend along the whole lateral surface of the fore-brain, whereby the connection with the brain here becomes severed. These cells are at first rounded, then become spindle-shaped and touch each other, so that they appear in connected layers. They are ranged mostly in two rows, but so that in one place a larger collection always shows itself. In my treatise I gave a figure(') of this, indicated this accumulation as a ganglion, and regarded it as the first rudiment of the first trigeminus ganglion. That it behaves like the rudiment of a ganglion I still hold, but I have come to doubt whether it goes into the first trigeminus ganglion or forms the first spinal ganglion, to be mentioned later. The determination is difficult, and requires more extended and especially more comparative investigations. But the whole mass of cells does not in every case collect itself into a compact ganglion, but it arranges itself in lines, which, after the appearance of the sense organs, extend both towards the nose and eye and also towards the hypophysial pouch. Later they unite, in the main, with the first trigeminus ganglion, whose branches they appear.

t Arch. f. Mikrosk. Anat., B<1. 35, 1890. Taf. XXFX, Fig. 39 g).

In the fore gill region^ which extends from the eye to the third primitive gill pouch, the process takes place otherwise. Here the mesoderm occurs in addition, which, until the time of the appearance of the dorsal root-borders at the brain, still shows an entirely epithelial arrangement. There are nowhere present detached cells which enter into the formation of connective tissue.

The root-border grows on rapidly to the dorsal border of mesoderm, and spreads out so that it lies cap-like upon the border cells of the mesoderm (Fig. 4). Then two tracts (Ziige) of cells separate, of which the inner proceeds between mesoderm and brain, while the other grows on laterad from the mesoderm between it and the epidermis. This latter course is characteristic of the fore gill region. It is wanting in the hind gill region and in the trunk.

As these tracts (Ziige) display separate rudiments, I choose for them exact designations. I call the inner tract, which remains in connection with the dorsal border of mesoderm and proceeds ventrad between brain and mesoderm, the dorsal spinal nerve ^ since tJiis rndiinent extends in the same way in all parts of the body; the outer tract I designate the branchial nerve (Figs. 5 and 6, nb).

The border (Leiste), and what proceeds from it, is not continuous in the fore gill region, but at the beginning is divided into three successive segments, which correspond to the regions of the trigeminus, acustico-facialis and vagus, and consists exclusively of elongated, serially arranged cells.

While the separation of the border into the tracts mentioned, the spinal and the branchial rudiments, takes place over the dorsal border of mesoderm — it takes place about the time of the appearance of the e3'e-rudiment — growths of the epidermis begin in three places; they are the trigeminus, the acustico-facialis and the vagus swellings. They lie laterad of the dorsal mesoderm, and arise, not simultaneously but successively, from before backwards. The method of formation of these swellings I have minutely described and drawn in my article. But I must here, on the the basis of later investigations, make some additions and corrections.

The trigeminus swelling, appearing close behind the eyerudiment, forms a projection (Fig. 4,^'/) directed entad and dorsad, and consisting of closely crowded cells, upon which, although still continuous, may be noticed two prominences lying the one behind and under the other. The root of the branchial nerve grows toward this swelling, unites with it by means of a tract of cells, and passes along, with another tract close by, growing in a ventral direction. The growth of these nerverudiments results partly from division of these cells, partly through the invasion of new elements from the dorsal brain-plate. At the point of junction of the root of the branchial nerve with the swelling of epidermis, there results a multiplication of the cells belonging to the nerve whereby two heaps of cells, corresponding to the two prominences on the swelling, arise, the elements of which are inserted between the epidermis cells of the swelling, so that later on they could not be distinguished according to their origin.

From this complex two ganglia are isolated successively with simultaneous separation from the epidermis, each of which consists of two parts, one epidermal and one arising from the dorsal brain-plate, of which the first part has been designated by me the lateral, the other as the medial ganglion (Figs. 5 and 7,^^/, ^"w). But the two parts are gradually merged into each other, so that finally no clear boundary between them can be pointed out. It is thus necessary to designate the whole body as one, and 1 propose the term '•'■ principaV ganglion (Hauptganglion) for it. There belong to the trigeminus two principal ganglia, formed in the same way, the Jirst and the second. The two are honiodynanious. I correct herewith my earlier view that the first trigeminus ganglion is exclusively of central origin, and has the same value as the medial part of the second trigeminus ganglion.(') A more complete series of stages has subsequently convinced me of the incorrectness of this view.

The first trigeminus ganglion lies before and over the second, can always be distinguished from this and is connected with the nerve-rudiments of the fore head.

The epidermal swelling next behind gives rise to the labyrinth vesicle and the lateral part of the yacialis ganglion, as likewise homodynamous parts, a portion of its cells also entering into the rudiment of the glossopharyngeus. Vesicle and ganglion arise in close connection, so that in the beginning of the invagination of the pit of the labyrinth, the ganglion is situated within, like a large knob, on the wall of the pit. It becomes further enlarged through proliferation of the cells of the wall. The root of the pertaining branchial nerve itself enters by way of addition, as well with the ganglion as with labyrinth vesicle, and stretches to one other part in this structure, lengthening in a ventral part. The ganglion acquires a median portion from the latter.

The third epidermal swelling, which belongs to the vagus, is more stmple than the two preceding. There proceeds from it a rounded, simple lateral ganglion, which, however, by means of the root of the pertaining branchial nerve connecting with it, acquires a considerable medial part and thereby becomes a principal ganglion.

During the formation of this principal ganglion, and before it has yet completely separated from the epidermis, there appear new growths of the epidermis. They lead, in like manner, to the formation of ganglia, without the connection with them of rudiments of sense organs, at least directly. These are the epibranchial ganglia (Figs. 4, 6, 7 ge). They arise singly, close above the three primitive gill pouches, and lie thus in a second series removed ventrally from that of the principal ganglia. The epibranchial ganglion appearing first is not the formost, but the one over the second gill pouch. At the end of the embryonic period, and after the release of the larvae, this process advances cephalad into the region of the trigeminus, and also caudad in proportion as the hind gill pouches successively arise. These ganglia thus exhibit regular branchiomerism, and those arising in the region of the trigeminus point to aborted anterior gill pouches.

t Arch. f. Mikr. Anat., Bd. 35, 1890, S. 538.

How the branchial nerves, passing along by the principal ganglia and proceeding to the visceral arches, connect with the epibranchial ganglia, I shall show later.

In the kind gill cegion, from the fourth primary gill pouch to the eighth, the development of the peripheral nervous system shows a less complicated course. The border (leiste) growing out from the dorsal brain-plate appears first as a continuous one, connects with the dorsal border cells of the mesoderm segments and sends a ventral extension between brain and mesoderm: there thus arises from it only the dorsal spinal nerve, the rudiment of branchial nerves remains apart from the border. There nevertheless arise, as already mentioned, in regular order from the epidermis, the epibranchial ganglia corresponding to the gill pouches of this region.

So long as the rudiments of the nerves consist of continuous chains of cells, it is not difficult to follow their course and establish the connections. But there comes a stage where, connected with the cells, fibrillfe appear and separate the cells, and with this difficulty ensues for the investigation, so long as the fibrill^e are not united into thicker cords. The latter has occurred after the release of the embryo, so the investigation is prosecuted on a firmer basis. One can then enumerate the roots in the different regions, and follow the ramifications of the distal nerves. The stage intervening between the first rudiment, consisting of continuous rows, and the later first evident compact nerve cords renders uncommonly difficult the determination of the question whether the rudiments and ganglia proceeding from the dorsal brain-plate and border respectively at any time give up their connection with the dorsal region of the brain. I assume this separation only for the region of the fore brain., where the rudiments also possess secondarily no connection with this region of the brain, but are united with the trigeminus and the mid-brain respectively. Behind this it does not occur, at least not up to the point of time when the formations of ganglia from epidermis begin and come forth in connection with the roots of the branchial nerves. With this question is bound up the other question of the final fate of the dorsal brain-plate. Do its cells advance in a body laterad and ventrad, or a middle portion of the cells of the plate remain in loco, while these cells intercalate themselves in the epithelial covering of the neural tube? According to my observations the latter takes place. A great part of the plate is applied to the formation of the peripheral nerves, but the remainder appears wedged in between the cells of the roof of the brain without the interruption of the connection wnth the peripheral parts.

I do not propose to discuss the histogeny of the nerves in this place, since the details are still not clearly enough established to admit of generalizations; but I may devote space for the view to which the embryo and the youngest larval stages of Petromyzon have led me. None of my observations contradicts the view, but rather everything indicates that the fibrill^e arise as processes of cells, but not merely from cells of the ganglia and central organ but also from those cells which, ranged in chains, form the first rudiments of peripheral nerves. This being accepted, it appears to me, further, most probable that the growth of the fibrillas in the dorsal nerves extends in both directions, centripetal as well as centrifugal. Thus, when the rudiments have attained the stage of formation at which they display fibrillge along with the cells, the cells appear moved apart from each other, and at both ends, the central as well as the peripheral, proceeding forth in fine filaments.

All other questions bearing further upon the peculiarities in this process appear to me at the present not ripe for dis^cussion. Yet I believe I may say one thing definitely, that the rudiments of the dorsal nerves, as w^ell in the earliest phase of the cell chains as also later, when fibrillae have already appeared, alw^ays show the connection with the central organ.

According to what has been hitherto communicated, there enter into the composition of the cranial nerves two systems, the spinal and the hrafichial. The first is common to the head and trunk; the latter appears exclusively in the head, is most developed in the fore gill region, and one part is produced into the hind gill region.

Concerning the spinal system of the head, I thus confine myself here to the dorsal rudiments, reserving the ventral spinal nerves for later mention. The complete interruption of the roots between the regions of the trigeminus, acusticofacialis and vagus self-evidently also affects the spinal system. It also divides, therefore, into three regions, of which the hindermost adjoins the spinal system of the trunk. Proceed-, ing from the root-border, the rudiment of a spinal nerve divides into two tracts. The lateral tract (zug) remains in connection with the dorsal border of mesoderm — I denote it as the dorsal branch of the dorsal spinal nerve — the median tract, or ventral branch of the dorsal spinal nerve, passes between mesoderm and brain towards the chorda, passes around this and arrives at the outer side of the aorta. At first consisting of serially arranged cells, this tract includes in itself the rudiments of the spi)ial gafiglia and of the sympathetic ganglia (Fig. 6).

So far as I have been yet able to discover, the spinal spinal system of the head does not keep pace in further development with the branchial system, but instead undergoes remarkable reductions.

The nerves of the branchial system are, in respect to their mode of origin, more composite. The rudiments proceeding from the root-border grow, with a participation in the principal ganglion then originating, over into the ventral region (Fig. ^, nd). It there connects secondarily with a portion proceeding from the distal end of the associated principal ganglion, of which I cannot definitely say whether it is of central or of epidermal derivation — that is to say, whether it is derived from the medial or lateral part of the ganglion, or from both. Then, later, when the epibranchial ganglia arise, further complications ensue. In conjunction with the formation of these ganglia, there appears a peculiar subepidermal layer of cells, which gradually spreads from the eye to the hindermost gill pouch, dzif remains conjined to thc ventral side.

If it were not preoccupied, I would suggest the name "hypodermis" for this layer, but, as it is, propose the term " neurodermis" (Figs. 6, 7, 10, nb). The point of origin of this structure is the vicinity of earliest epibranchial ganglion, dorsad and cephalad of the second gill pouch. At the lateral line, i.e., the outer boundary between the dorsal and ventral region, the neurodermis is not strongly developed; here it consists of several layers of cells which form an inwardly projecting ridge, but in general it remains one-layered and consists of closely arranged but disconnected epithelium-like cells, with a prevailingly cylindrical form.

Note. — The figures which are referred to in this paper will be collected in plates at the end of the article.

[to be CONTINCE]).]

Cite this page: Hill, M.A. (2021, September 24) Embryology Paper - The development of the cranial nerves of vertebrates 1 (1891). Retrieved from

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