Paper - The development of the cranial nerves of vertebrates 2 (1891)

The Development Of The Cranial Nerves Of Vertebrates

von Kupffer C. The development of the cranial nerves of vertebrates. (1891) Translated by Oliver S. Strong J Comp. Neurol. 1: 315.

Prof. C. von Kupffer.

Tracing their origin, these cells are seen to proceed from the epidermis. The latter thickens by elongation of its elements, which then divide transversely, after which the ental layer of daughter cells do not reassume their epithelial arrangement, but constitute the special sub-epidermal layer or neurodermis. The latter has in any case a close relation with the development of the peripheral part of the branchial nervous system, evidence of which is furnished by the fact that the thickening of the epidermis, which precedes the development of this structure, is derived from the rudiment of the epibranchial ganglion.

It is cells of this layer which furnish the first commissures connecting the epibranchial ganglia with each other, as well as with the preformed branchial nerves and with the definitive (principal) ganglia. It may, therefore, be said that the epidermis contributes to the development of the peripheral branches of the branchial system, but whether these cells play a r6le in the formation of the fibrillae, or simply have a secondary significance, cannot be determined at present.

CRANIAL NERVES OF YOUNG AMMOCCETES.

After this exposition of the main features in the development of the cranial nerves, I pass on to their description in young Ammocoetes, which, when fixed (sublimate, alcohol), measure 3^-3^ mm. While living they might have been fully 4 mm. The stage of development of these specimens, upon which I base mv description, is as follows: There are seven pairs of gill pouches present; the hindermost (eighth) pair is in formation. In the foremost, obliquely placed and temporary pair of pouches, the withdrawal of the endoderm from the epidermis has already taken place and the mesoderm interposed. The diaphragms in the pouches are not yet formed; outer spiracles are still wanting throughout. The septum between the oral cavity and the branchial gut is not yet perforated, but is thinned, and the formation of the stomodcBum from pouches, described by Dohrn,(') whereby the free surface of the velum is enlarged, has set in. There is as yet no pigment in the eye, the lens is constricted off, and the recessus labyrinthi extends dorsad to the exit of the roots of the facial. There exist three pronephric canals with funnels formed, and on each side a large glomerulus. The pronephric duct reaches the hind gut.

Translated for this journal, from advance sheets, by Oliver S. Stroni;, Fellow in Biology in Columbia College.

BRANCHIAL SYSTEM.

I begin with the description of the branchial system of the cranial nerves of this larva, referring to Fig. S, which is drav^^n from three sagittal series of sections, and shows the roots, ganglia and peripheral nerves of the system projected on the median plane. One sees in the figure two rows of ganglia, i.e., dorsally the row of huge or principal (Hauptganglion) ganglia (I-V), and ventrally, over the gill septa (gill arches), the epibranchial ganglia (1-12) bound by commissures into one cord. A third row of ganglia is shown in the drawing between the gill pouches.

1. Rcoion of the Trigctuirms. — The two principal ganglia of this region are plainly set oft' from each other. The first

I DoHKN, XII, "Studies," 1888, p. 238-239.

is somewhat smaller than the second, and has an approximately triangular shape, the base directed dorsad. It lies over the eye. From the fore corner there go out two stout nerve trunks, which proceed in an arch cephalad and ventrad. In the ganglion two portions may be distinguished. Tlie dorsal, broader part is traversed by fibrilLne which proceed, in direction, from the roots to the branches; in the ventral, tapering part no fibrillre can be perceived among the nerve cells.

The second principal ganglion, more voluminous than the first, has also a stouter root (perhaps already two). It lies over the stomodseum and likewise displays two divisions, which have the same relations as those of the first principal ganglion; fibrillfe traverse the fore dorsal part, the hinder part appear free of fibrillas. From the fore part there go close together the two branchial nerves, the N. maxillaris and N. mandibularis. Both consist of a compact cord of fibres, which contains nuclei within, and at the surface shows an envelope of cells.

The epibranchial ganglia of this region show a continuous chain which impinges cephalad upon the lens, so thai it appears as the foremost part of the chain. One can distinguish between the lens (it not being reckoned in) and the N. mandibularis, three parts of the chain, marked oft' by constrictions, which may be designated the first, second and third epibranchial ganglia. The first is inserted slightly under the lens, the second projects somewhat dorsally and is directly connected with the first principal ganglion. The third epibranchial ganglion lies at the lateral side of the origin of the NN. maxillaris and mandibularis, and stands in broad connection with the cell mass of the second principal ganglion.

2. Region of the Acustico-Facialis. — The fi^cial ganglion and the auditory vesicle of the principal ganglia belong to the series. The principal ganglion of the facial projects far forward over the auditory vesicle, and its fore end lies under the hinder surface of the second principal ganglion of the trigeminus. It reaches around the auditory vesicle on the median and ventral sides as far as its middle, and here ends in a point. The contact w^ith the wall of the auditory vesicle is very close.

I assign to the same region two ganglia of the epibranchial chain, namely, those lying in front of the first and second gill pouches, and which, numbered from before, would be four and five. The fifth epibranchial ganglion is immediately connected with the principal ganglion of the facial, and participates in the composition of the N. branchialis, a massive cord proceeding chiefly from the principal ganglion into the hyoid arch. The diminished fore end of the principal ganglion extends into the commissure which connects the fifth with the fourth epibranchial ganglion. At this stage a short nerve "anlage" proceeds from the latter, which is produced into the substance of the mandibular arch, superficially, in a ventral direction. But this fourth epibranchial ganglion occupies an intermediate position, and is connected both with the principal ganglion of the facial and the second principal ganglion of the trigeminus. While I assign it provisionally to the facial region, this view needs to be proved by further investigations as to its later fate.

I have, from earlier stages, represented as acusticus the hinder portion of the one continuous branchial root of this region, (') which is connected with the wall of the auditory vesicle at the base of the recessus labyrinthi, and has, at that time, developed no ganglion. It has not essentially changed from there on to the stage now under consideration. The acusticus, too, only shows here this one place of connection with the auditory vesicle. Although cells may be seen between its fibrilhe and in connection with them, they cannot yet be called a ganglion.

3. Jxcgion of ihe I 'agns Group. — As belonging to this

I Arch. f. Mikr. Anat., 1890, Bd. 35, p. 543.

region I have described, from the stage of development reached in the days immediately preceding the exit of the embryo:(') (i) A large isolated lateral ganglion arising from the epidermis, and located over the second and third gill pouches; (2) a medial ganglion proceeding from the rootborder (Wurzel Leiste) and uniting with the latter; thus there are, according to my present terminology, the components of a principal ganglion of the vagus; (3) epibranchial ganglia over the second and the following gill pouches. A lateral ganglion assigned to the glosso-pharyngeus is developed between the auditory vesicle and the vagus, and not isolated from the epidermis. I supposed, therefore, that the glosso-pharyngeal ganglion described -by Scott and Shipley is an epibranchial ganglion. ('■) At the same time I pointed out that there is no sharp division between the facial group and that of the vagus at this stage. The epibranchial ganglion lying over the second gill pouch received a verv noticeable addition from the root-border, consisting of cells and fibrillas, but at the same time a nerve originating from the facial root sinks into this ganglion, which I called the ramus recurrens of the facial.

In AmmoccEtes of 4 mm. the relations are much clearer, the individual parts are more separated, and at the same time there has taken place a displacenient laterad which renders easier the comparison with the relations in older Ammoccetes. The epibranchial ganglia experience a transference caudad, so that they are no longer located over the gill pouches, but are over the corresponding gill septa (visceral arches), i.e., the ganglion formed over the second gill pouch now lies directly over the septum between the second and third gill pouches. The auditory vesicle in larva? of 4 mm. is situated over the second gill pouch, projecting somewhat beyond it both caudad and cephalad. As the principal ganglion of the facial lies close to the wall in the fore half of the auditory vesicle, so is the ganglion of the glosso-pharyngeus in close contact with its caudo-ventral wall, and has fused with the portion of its cells which I have mentioned and drawn as the sickle-shaped investment of this part of the wall of the vesicle.(') This cell-girdle, up to the time of the exit of the embryo is continuous with the mass of the principal ganglion of the facial, and I have accordingly assigned it to the latter. But it changes later. In larvje of 4 mm. the separation is completed, and the cell group under consideration has by this time connected itself with the glossopharyngeus. It thus comes to pass that the continuous cell mass, which originates from the epidermis in closest contact with the labyrinth pit and is further augmented by the cells of the wall of the latter, embraces the lateral portions of two ganglia, the larger fore part going over to the principal ganglion of the facial and the smaller hind part to the ganglion of the glosso-pharyngeus. Along with this the glossopharyngeus moves out of the particular place which I believe must be assigned to it originally, before the separation of the ganglion mass adjoining the labyrinth vesicle into two parts has been completed.

1 Ibidem, p. 544.

2 Ibidem, p. 552.

As the glosso-pharyngeus is now, it consists of a stout fibrillar root, which is evidently separated from the acusticus but unites with the.vagus root lying caudad. The root enters an elongated ganglion whose medial part, likewise present from the first, has united secondarily with the lateral part which was joined to the labyrinth vesicle. This principal ganglion, extending further, now fuses with the epibranchial cord, so that it completely takes in the sixth epibranchial ganglion. At the same time, however, it connects itself, by a tract (Zug) directed cephalad, with the fifth epibranchial ganglion. The latter is thereby closely related both to the facialis and to the glosso-pharyngeus.

The relations of the vagus, in the strict sense, when compared with the earlier stages, have changed the least.

I Arch. f. Mikr. Anat., i8qo, p. 524, Figs. 54, 74.

Its large principal ganglion, arising typically, lies above the septum between the third and fourth gill pouches and over the fourth pouch itself. The short, stout, single root is mostly fibrillar, but also contains cells, both in the interior and as an envelope outside. It sinks into the cephalo-dorsal angle of the ganglion. The hind point of the approxiniately triangular ganglion extends into the N. lateralis, entirely lacking ganglia, which ends in the caudal half of the trunk in a swelling of the epidermis. The cephalo-ventral angle of the principal ganglion sends out the stout N. branchio-gastricus, rich in cells, which connects itself with the seventh epibranchial ganglion (numbering from before). Five more ganglia lie behind this in the epibranchial cord. There are thus found in the whole chain, which extends from the eye to behind the eight gill pouches, altogether twelve epibranchial ganglia.

THE BRANCHIAL NERVES.

I begin with those lying caudad, where the relations are simplest. The hindmost five branchial nerves have the same relations. Each one arises as a cord from the appropriate epibranchial ganglion, and is connected by means of a second more slender cord with a sympathic ganglion of the spinal system. It proceeds then ventrally into the gill arch and divides into a cutaneous and a muscular branch. The cutaneous branch is the foremost, and connects itself with a rounded protuberance of the epidermis projecting entad. The muscular branch accompanies the arch of the aorta ventrad and ramifies further (Fig. 9). The external spiracula (gill openings), which are formed behind the pertaining gill pouch, have arisen. Thus the cutaneous branches are shown to be the rami pra;trematici, and the epidermal prominences small separated ganglia, which I will denote as ganglia praetrematici.

The sixth branchial nerve, numbered from behind, arises from that epibranchial ganglion which the N. branchiogastricus of the vagus enters. Here, as well as with the branchial nerves lying cephalad, it can be established that their most important part is derived from the principal ganglion, and that the portions derived trom the epibranchial and sympathic ganglia are the smaller.

The branchial nerve of the glosso-pharyngeus, the seventh from behind, and that of the facialis behave like the foremost one of the vagus. All these nerves divide within the gill arch into the cutaneous and muscular branches, the first of which fuses with an epidermal prominence, the subsequent ganglion praetrematicum.

In the region of the four anterior epibranchial ganglia this arrangement is destroyed, owing to the stomodasum, and the interpretation of the peripheral nerves present here is difficult. Three nerves come into consideration, namely: (i) A short nerve springing from the fourth epibranchial ganglion (numbered from before), which proceeds behind the N. mandibularis to the epidermis and ends in a small ganglion (probably the r. mand. ext., Fiirbringer); (2) the N. mandibularis, which, as a stout fibrillar cord, leaves the second principal ganglion of the trigeminus and derives the greater part of the fibrillae directly from the branchial root; a more slender cord from the third epibranchial ganglion joins this; (3) the N. maxillaris; this arises from the principal ganglion and the second epibranchial ganglion. I must let it remain undetermined whether the first epibranchial likewise has a share in this nerve. The N. maxillaris divides into branches for muscles in the upper lip, for the side wall of the stomoda'um and for the skin of the lip. A twig proceeding along the skin ends in a ganglion lying close under the epidermis, which behaves entirely like the praitrematic ganglia of the gill region.

There are thus always present in the region of the trigeminus small ganglia of a third series, which I might annex to the praetrematics of the gill region, and it is worth noticing that such a one lies in front of the stomodaeum.

Since at least one epibranchial ganglion participates in the formation of the N. mandibularis, as well as of the N. maxillaris, I regard both nerves as homodynamous to at least one branchial nerve, but reserve a final judgment as to their value.

I cannot clearly demonstrate a participation of the first epibranchial ganglion, impinging upon the lens, in the formation of peripheral nerves.

SPINAL SYSTEM OF CRANIAL NERVES.

The determination of the parts of this system encounters great difficulties. The somites, which ^re present only a short time between the ear and eye, already dwindle away a perceptible time before the exit of the embryo, and with them the dorsal branches of the dorsal spinal nerves. The principal ganglia of the branchial system, the eye and the lateral muscles of the head growing cephalad take up so much space that the spinal nerves have to be sought in narrow interspaces. In every case they are less developed than those of the branchial system. One does not meet compact cords in the developmental stage under consideration, but only loose strands of fibrillae connected with cells. One applies himself with more advantage to the ganglia than to the roots for the determination of their number and arrangement.

One encounters the foremost ventral spinal nerve, the root and the little ganglion of a dorsal spinal nerve, which I regard the foremost almost in a single transection (Fig. 10, vs, ds). This spinal ganglion lies between the secondary optic vesicle and the brain. In a cross section close behind this there lies a second ganglion, ventrad from the first, on the outer wall of a blind extension of the aorta. It is connected with the first, and I can regard it only as the foremost sympathic ganglion.

The foremost ventral spinal nerve is a short fibrillar cord, with cells disposed in and on it, which springs from the ventral aspect of the mid-brain close outwards from its basal plate. It proceeds between the fore end of the chorda and the aorta, and approaches a hollow epithelial cord which serves to connect with each other, under the end of the chorda, a pair of bodies rich in yolk and lying laterally. There can be not doubt but that these two bodies are the head cavities which Dohrn(') describes and from which he derives the eye-muscles. If, however, Dohrn made his observation upon these, the median piece connecting them would not be a ventral but a dorsal structure, because the carotis lies beneath it; so I must call attention to the fact that this connecting part has its location over the carotis, indeed, but under the blind foremost terminal piece of the aorta. Recently Dohrn, departing from his earlier view, states that the middle connecting part originates, in fact, from the median fusion of two entirely distinct myotomes;(-) with which I cannot agree. I consider the two head cavities under discussion, together with the cord uniting them, the foremost part of the anterior endodermal pouch which in this stage of development has even separated from the hind part of the pouch.

Peculiar as is the behavior of the nerve now in approaching this connecting piece destined to atrophy, I nevertheless believe it may be considered as the oculomotorius, since the paired praechordal head cavities, made single by the connecting piece, always participate in the formation of the eyemuscles.

I must for the present leave undetermined whether a cord which springs dorsally from the mid-brain, between the roots of the first and second principal ganglia of the trigeminus, and behind the eye approaches the second epibranchial ganglion, persists as an eye-muscle nerve (com p. Fig. 8). Should this conjecture be established, this nerve would not belong to the spinal but to the branchial system.

1 XII Stuilie. Mitteil. aus d. Zool. Station zu Neapel, Bd. VIII, 1887, pp. 325, 328, 330.

2 XV .Studie. Mitteil. aus. d. Zool. Station zu Neapel, Bd. IX, p. 332, Anmerk.

If one can say that the foremost pair of dorsal and ventral spinal nerves are situated within the vicinity of the first principal ganglion of the trigeminus, in the same way one meets a second pair of dorsal spinal ganglia, connected with its sympathic ganglia, mesad from the second principal ganglion of the same region and in the same transverse plane with the exit oi the N. mandibularis from the principal ganglion just mentioned. I can state nothing definite concerning the terminal twigs belonging to this pair.

The same difficulty in following out the spinal nerves exists in the region of the facialis. The large principal ganglion and the labyrinth vesicle take up the space between the epidermis and brain almost entirely, and push the remaining elements apart. I have not been able to demonstrate a dorsal spinal nerve in the whole course, in a 4 mm. larvs, but have, indeed, a spinal ganglion, wedged in between the principal ganglion of the facialis and the chorda, and also a long sympathic ganglion, lying close to the aorta, which gives off fibres to the branchial nerve of the facialis. This spinal ganglion probably fuses later with the principal ganglion.

The pointed fore end of the first myomere of the body pushes up close to the hind end of the principal ganglion of the facialis, and even inserts itself slightly under the ganglion. The lateral muscles of the head do not first proceed from this, but from the second myomere, close behind the first branchial nerve of the vagus. Here, over the fore end of the second myomere, for the time being, the regular series of the spinal ganglia and spinal nerves of the trunk also begins.

This first myomere of the 4 mm. Ammocoetes lies thus in the region of the glosso-pharyngeus, with its fore end over the second gill pouch. I have not found a ventral spinal nerve connected with the myomere, but have found a dorsal spinal nerve with a slight ganglion, and observed its dorsal branch approach the dorsal border of the myomere and its ventral branch proceed on to uniformly small sympathic ganglion. I do not know^ whether this myomere persists. But in any case the pertaining spinal nerve would not be reckoned among the cranial nerves.

I have only succeeded in demonstrating three pairs of dorsal and one pair of ventral spinal nerves of the head, and that over an extent to which belong five pairs of epibranchial ganglia.

The spinal system is therefore in Ammocoetes, at least in the stages of development known to me, of little value for the determination of the segmentation of the head. The epibranchial ganglia furnish the surest basis for this.

I have enlarged so particularly on the cranial nerves of Ammocoetes because, on the basis of what has been communicated, I am of the opinion that here very primitive relations exist, which furnish important hints for the criticism of the cranial nerves of Gnathostomata. Three-fold phenomena determine me to this view: First, the far-extending formation of the epibranchial ganglia in the trigeminus region; then the close proximity of the letis to this chain of ganglia^ whereby a new light falls upon the phylogeny of the eye; and, finally, the very important — probably preponderating — part which the epidermis plays in the formation of the principal ganglia. As the auditory organ is referred to the series of principal ganglia^ the eye appears to belong to the epibranchial series.

The works, already cursorily mentioned, of Van Wihje, Froriep and Beard furnish guaranty that the developmental processes, which I have described in Ammocoetes, also essentially recur in Gnathostomata. These named have not seen the separation of the first cranial nerve rudiment (Anlage) into spinal and branchial nerves, cephalad of the vagus, but the formation of epibranchial ganglia from elasmobranchs on to mammalia is clearly established through their works. There remains on this side the evidence that the epidermis also participates in the principal ganglia.

There cannot be the least doubt but that the fusions, described by Van Wihje, of the ventral twigs of the facialis, glosso-pharyngeus and vagus with thickened places in the epidermis on the upper hinder wall of the pertaining gill clefts correspond to the places of formation of the epibranchial ganglia. Besides the local relations to the gill clefts or pouches, the circumstance that these places are described as starting points for the branchial terminal twigs: the rami postand praetrematici also argue for this. In sagittal sections these terminal twigs appear, in fact, as outgrowths of these ganglia, while cross sections teach that the epibranchial ganglia have, indeed, an essential but not exclusive share in the formation of the NN. branchiales.

For a time I was of the opinion that the more dorsally situated places of fusion of the dorsal branches of the cranial nerves with the epidermis, which Van Wihje mentioned, could be brought into connection with the formation of the principal ganglia. But on closer examination of the relations, this conjecture proves untenable. These dorsal branches in Selachians are purely cutaneous sensory nerves; the thickened patches of epidermis furnish the lateral organs, remaining in connection with the epidermis, and their peripheral nerve apparatus. On the other hand, the lateral portions of the principal ganglia have nothing to do, directly, with the sense organs; they separate cleanly from the epidermis, which shows thereupon a marked thinning, and move deeper within.

Beard has occupied himself more particularly than Van Wihje with these epidermal formations; only it is difficult to get a clear idea of the particulars from his publications, since this active investigator is so filled with his hypothesis of the branchial sense organs that his exposition of the development of the cranial nerves aims before all to bring its processes into harmony with this hypothesis.

From no place in his numerous writings does it clearly emerge that he has, in general, seen or noticed the formation of the lateral portion of the principal ganglia from the epidermis. In one place(') in his last large publication but one he says, much more explicitly, that the nerves growing out from the border (Leiste) connected themselves at the level of the chorda with the epidermis, which statement points to the epibranchial and not to the principal ganglia. Then, it is said further on, the dorsal branches or supra -branchial nerves arose at the same time xvith the fr(£branchial nerves, along with the separation from the epidermis of the ganglia that arose in the region pointed out — that is, after the origin of the epibranchial ganglia. This expression, also, does not perm.it us to suppose the formation of the dorsal branches connected with the principal ganglia, since the latter arise noticeably earlier than the epibranchial ganglia.

Also in the last treatis of Beard's, furnished with numerous figures, it is said, in accordance with the above-mentioned expression, that the cranial ganglia corresponding to the spinal ganglia received additional form-elements from the lateral epiblast over the gill clefts and at the height of the chorda. To draw a conclusion from this. Beard might not have seen the formation of the lateral portions of the principal ganglia, and the lateral ganglia in his and in my sense would not be identical, but Beard's lateral ganglia would correspond to my epibranchial ganglia. Nevertheless, some of his figures show that in the elasmobranchs also the epidermis forms ganglia in two well-distinguished series lying apart one over the other, lateral and epibranchial. I refer thereupon to the ^uart. Jour. Mic. Se., Vol. XXVI, 1886, Plate IX, Figs. 20 and 23, on the facialis of Torpedo. Probably the principal and epibranchial ganglia mingle very early in Torpedo, whereby the perception of their separate origin is rendered difficult. This being the case, Beard's lateral ganglia would correspond to the lateral and epihranchial ganglia together in my sense. A renewed investigation of the development of the , cranial nerves of elasmobranchs is necessary to obtain clearness here.

I Quart. Jour. Mic. Sc, Vol. XXVI, 1886, p. loi.

Froriep's communications are much more intelligible. In the youngest cow embryos on which he began his investigations, the principal ganglia were already formed and removed from the epidermis, so only the formation of the epihranchial ganglia could be treated of, the rudiments (Anlage) of which exist in Froriep's " gill cleft organs." The thickened patches of epidermis behind the eye in young cow embryos, mentioned by him, I might pronounce without hesitation to be the rudiments of the foremost epihranchial ganglia.

So that I could express from personal inspection an opinion upon the mode of formation of the cranial nerves in Amniota, I have commenced a piece of work in the Institute of this place upon bird embryos, which, begun not long ago, already has led to the result that there exists essentially a complete agreemefit zvith the processes in Cyclostomes . The duck appears to furnish an especially suitable object. It has become apparent that the rudiments of the cranial nerves proceeding from the root-border ( Wurzelleiste) divide into the spinal and branchial nerves, and that these branchial nerve rudiments, while they are yet mainly composed of cells, grow distally between epidermis and proto vertebrae, and on the one hand fuse with the epidermis for the formation of the principal ganglia, on the other hand, after the separation of the principal ganglia from the epidermis, enter into a second connection with it over the gill pouches.

This work has not progressed far enough to enable me to go into particulars, but this much may be said, that in the trigeminus region also the typical mode of development is preserved, since in the formation of the first principal ganglion of the trigeminus in the duck there can be demonstrated a very considerable participation of the epidermis. In the chick with nine to ten protovertebrse, we see the root-borders reach the dorsal border of the mesoderm. Duck embryos with eleven to twelve protovertebrfe show the ganglion of the trigeminus in connection with a lateral swelling of the epidermis. Somewhat later the connection with the epibranchial ganglion appears. In the daw with twelve protovertebrre I saw a branchial nerve connected with the epidermis in both places at the same time.

You will grant that it would be altogether premature for me to express an opinion now, more or less probable, upon the changes which the scheme of the nerves of the head of vertebrates here presented experiences up to the completion of development. The reductions, fusions, solutions of continuity and secondary connections appear to vary according to the class in very many ways.

A comparison of the representation of the branchial nervous system in the AmmoccEtes (Fig. 8) of 4 mm. with a diagram of the cranial nerves of the adult (Fig. 11) shows you how important these changes may be. I have constructed this diagram after Ahlborn's and Julin's drawings, taking into consideration also the statements of Max Fiirbringer and Wiedersheim. To present a better general view, the oculomotor nerves and hypoglossus are omitted.

The whole anterior portion of the epibranchial cord, cephalad of the vagus, appears to have appeared, but is still represented by the ramus recurrens and ramus anterior of the facialis. The latter, behind and under the eye, possesses the spindle-shaped ganglion discovered by M. Fiirbringer. I conjecture this ganglion to be the remant of the foremost epibranchial ganglion or a complex of such ganglia. One might express it in this way: That in the course of development the facialis annexes all those portions of the epibranchial cord lying cephalad of the vagus. Whether the commissure, described by Ahlborn, between the first trigeminus ganglion (Gn. ophthalmicum) and the facialis ganglion (v. Fig. 11) has also been derived from the epibranchial cord, and the latter has consequently divided as it proceeds cephalad, cannot be finally answered now, with probability, either way. But I must call attention to the fact that I did not see direct commissures between the principal ganglia, so that there is a certain warrant, pending further disclosures, in deriving all commissures in general between the vagus and trigeminus regions from the epibranchial cord.

DESCRIPTION OF PLATE XXII.

Fig. 1. It, neural cord: z, 'twixt cord (Zwischenstrang). ^^ .

Fig. 2. //, neural cord; d P, dorsal brain-plate. ^5°.

Fig. 3. h, fore brain; a, rudiment of eye; d P, dorsal brain-plate; 11, rudiment of nerve; g, ganglion, ^oo

Fig. 4. //, mid brain; /, root-border; jn, mesoderm; r//, chorda, d, gut; g/, lateral ganglion, ge, epibranchial ganglion, ^oo

Fig. 5. //, mid brain; ch, chorda; d, gut; 711, mesoderm; /, rootborder; Jis, dorsal spinal nerve; nb, branchial nerve; gl, lateral ganglion; gvi, medial ganglion.

Fig. C. //, hind .brain; /, root border; 11 s, dorsal spinal nerve; nb, branchial nerve; gl, lateral ganglion of vagus; ge, epibranchial ganglion; ^.T, sjmpathic ganglion; ;/rf, neurodermis. 200

Fig. 6. h, hind brain; ch, chorda; d, gut; ;«, mesoderm; ns, dorsal spinal nerve; nb, branchial spinal nerve; gl, hind end of lateral ganglion of vagus; ge, epibranchial ganglion; nd, neurodermis.

Fig. 7. h, fore brain; gin, medial ganglion; gl, lateral ganglion, both belonging to the I principal ganglion of the trigeminus; ge, epibranchial ganglion; ;;.?, dorsal spinal nerve; ;/f/, neurodermis. *J°.

Fig. 8. Branchial nervous system of an Ammocoetes 4 mm. long, projected on the median plane, about ^J^. A, eye; N, nose; O, ear; /, first, //, second principal ganglion of the trigeminus; ///, principal ganglion of facial; /I', principal ganglion of glosso-pharyngeus, fusing ventrally with the sixth epibranchial ganglion; V, principal ganglion of vagus, first, seventh and twelfth epibranchial ganglia; K^-K^, gill pouches; ch, chorda; /, nervus lateralis. Going out from the epibranchial ganglia and proceeding ventrally between the gill pouches are the terminal branches of the branchial nerves, forking into the ramus posttrematicus and pra?trematicus. The rr. prsetrematici end in the structure with a knob, the ganglion praetrematicum, about half way up the gill pouch. The foremost of these ganglia is before the stomodseum, on a twig of the maxillaris. The small circles behind the second to the eighth gill pouches, between the rr. postand prietrematici, show the locations of the later appearing spiracula externa.

J^iff. 9. Ii, hind brain; a, aorta; «/, muscle; I', principal ganglion of vagus; 7, seventh epibranchial ganglion; g-, rudiment of a gang, prsetrematicum, with which the r. preetrematicus is connected. Inwards from it twigs of the r. posttrematicus. s, a sjmpathic ganglion; iid, neurodermis. ^Y^-

J^ig^10. h, mid brain; A, eje; cli, chorda; A', prtechordal head cavity, connected by means of the hollow connecting cord with that of the other side; w, stomodseum; vs, foremost ventral spinal nerve; ds, foremost dorsal spinal nerve; nd, neurodermis.

Fig. 11. Dorsal cranial nerves of adult Ammocoutes, i.e., Petromyzon, semi-diagrammatic. The ganglia, especially those caudad, are somewhat separated, so as not to overlap in the figure. A, eye; iV, nose; O, cartilaginous auditory capsule; A', foremost gill cleft; /, first, //, second principal ganglion of trigeminus; ///, principal ganglion of facialis; /V, principal ganglion of glosso-pharyngeus; I', principal ganglion of vagus; 1, first, 7, seventh epibranchial ganglion (comp. Fig. 8); ;-«, ramus anterior; ;-/, ramus posterior; rr, ramus recurrens of the facialis.

Note. — The fractions representing the amplification of the figures are those accompanying the original. All the figures have been somewhat reduced during reproduction. —Ed.