Paper - The segmental value of the cranial nerves (1882)

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Marshall AM. The segmental value of the cranial nerves. (1882) J Anat. Physiol. 26(1): 94–99. PMID 17231431

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This historic 1882 paper by Marshall is an early description of the development of the cranial nerves. See also: Marshall AM. The morphology of the vertebrate olfactory organ. (1879) Quarterly Journal of Microscopic Science. 19: 300–340. Marshall AM. Thyro-Glossal duct or “canal of His”. (1881) J Anat. Physiol. 16(3): 305–354. PMID 17231961 Marshall AM. The segmental value of the cranial nerves. (1882) J Anat. Physiol. 26(1): 94–99. PMID 17231431 Marshall AM. Vertebrate Embryology: A Text-book for Students and Practitioners. (1893) Elder Smith & Co., London. Historic Embryology Arthur Milnes Marshall (1852–1893) at Cambridge in 1879 historically first described this embryonic region. In his study of dogfish and chicken brain development, and identified it as "neural crest". See neural crest history and the original 1879 article. Wilhelm His (1831-1904) in 1868 also described in the chick embryo the early neural structure that would form neural crest. Modern Notes: cranial nerve 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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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

The Segmental Value of the Cranial Nerves

Arthur Milnes Marshall

By A. Milnes Marshall , M.A., D.Sc,

Fellow of St. John’s College, Cambridge, Professor of Zoology in Owens College. (PLATE X.)

Introduction

Whether the nerves arising from the brain are directly comparable to those taking their origin from the spinal cord, and, if so, to how many pairs of the more symmetrically arranged spinal nerves the cranial ones are equivalent, are questions which have attracted the attention and exercised the ingenuity of many of the greatest anatomists, and ones which have been answered in the most varied senses by the different writers who have attempted to grapple with their difficulties. So long as the problems were attacked from the morphological side alone, as was the case with all the earlier attempts to solve them, the answers obtained were vague, inconclusive, and mutually contradictory; but since the clear light of embryology has been directed upon them the clouds of uncertainty have been to a very considerable extent dispersed, and there is now, especially amongst those who have most recently dealt with these questions, a very considerable and satisfactory agreement as to the main outlines of the answers to be given, although in many points of detail there is still much discrepancy between the several accounts,

The present paper is an attempt to set forth the actual position of these problems, and the leading phases through which they have passed in their gradual maturation. In preparing it I have made use of the investigations of others, so far as known to me, as well as of my own published in this Journal and elsewhere.

• A list of the works consulted is given at the end of this paper.

Historical Sketch

The older writers relied exclusively on anatomical evidence in dealing with the problems before us, and their determinations were rather of the nature of guesses than logical endeavours to grapple seriously with the difficulties encountered. Moreover, in the great majority of cases their judgment was influenced in a very prejudicial manner by preconceived ideas on the morphological constitution of the skull.

Inasmuch as these older theories are all based on the same arguments, and differ from one another ouly in points of minor importance, it will be sufficient to take one of them and examine it critically, For this purpose I select the theory advanced by Stieda, the most recent, indeed the only recent, advocate of the views in question.

Stieda, in attempting to solve the problem of the segmental value of the cranial nerves, commences by stating that as he accepts Oken’s theory that the skull consists of three vertebre, the number of pairs of segmental cranial nerves must necessarily be two; viz.,a pair leaving the skull between the first and second skull-vertebree on either side, and a pair emerging between the second and third skull-vertebre, the nerves passing out between the skull and the first cervical vertebra being universally considered, when present, the first pair of spinal nerves.

Having in this very summary manner determined the number of segmental cranial nerves, Stieda proceeds to divide the nerves actually present into two groups in accordance with this determination. He first rejects the nerves of special sensation, 4.¢., the olfactory, optic, and auditory, on the ground that embryology shows them to be really parts of the brain, and therefore not directly comparable with the other nerves.

Concerning the remaining nine pairs of nerves still left for consideration, he holds that the most reliable evidence is afforded by the fact that in certain groups of animals some of these nerves do not arise independently from the brain, but are represented by branches of other nerves.

1 Stieda, Studien idber dvs centrale Nervensystem der Wirbelthiere, Leipzig, 1870. Separat-Abdruck aus der Zeitschrift fiir wissenschaftliche Zoologie, Bd. xx. p. 166, seg.

Reasoning from these data, Stieda comes to the conclusion that the component factors of his first cranial segmental nerve are the third or oculomotor, the fourth or trochlear, the fifth or trigeminal, the sixth or abducent, and the seventh or facial nerves ; and that of these the third, fourth, sixth, and seventh nerves, and the motor root of the fifth together represent the anterior or motor root, while the sensory portion of the fifth nerve is the representative of the posterior or sensory root. In support of these conclusions he adduces the following arguments :—

1. That the three eye-muscle nerves and the facial nerve may sometimes be replaced by branches of the trigeminal,! and therefore may be considered as belonging primarily to that nerve.
2. That the three eye-muscle nerves, the facial nerve, and the portio minor of the trigeminal behave with reference to their origin from the brain like the anterior roots of the spinal nerves ; the portio major of the trigeminal, on the contrary, like a posterior root: meaning by this, the relations of the nerves in question to the nuclei of origin within the substance of the brain.

The second or posterior cranial segmental nerve he considers to be made up of the ninth or glosso-pharyngeal, the tenth or vagus, the anterior roots of the eleventh or spinal accessory, and the twelfth or hypoglossal nerves; the ninth, tenth, and anterior roots of the eleventh pair making up the posterior root, and the twelfth nerve representing the anterior or motor root, the main grounds of determination being the same as those relied on in the case of the supposed first nerve.

I have quoted Stieda at some length mainly in order to direct attention to the nature of the evidence on which he attempts to solve the question. The main points on which he relies are contained in the passages I have italicised above, viz., (1) that the nerves of special sense are contrasted with the other cranial nerves as being, properly speaking, parts of the brain and not nerves in the strict sense of the word ; and (2) that in certain groups of animals one or more of the cranial nerves may lose their more usual independent character, and appear as, or be replaced by, branches of some other nerve; and further, that this 1s to be taken as indicating that.the nerves in question were originally branches of this other nerve, and that their independent origin from the brain, when it does occur, is a secondarily acquired feature.

1 All the cases in which this replacement is alleged to occur will be discussed later on in this paper.

Now, these two points are of primary importance, forming, as is at once seen, the whole basis of Stieda’s argument, and in relying on them he is very far from standing alone. Indeed, until some five or six years ago their correctuess has been assumed, either tacitly or explicitly, by the great majority of those who have dealt with the question, including some of the most eminent anatomists of the time, such as J. Müller Arnold, Langer, Gegenbaur, and, though in a somewhat less positive manner, Huxley I direct attention to this at once, because we shall find further on that there are very strong reasons for holding that neither of the points in question is really correct. I have taken Stieda as the most recent representative of a school to which C. V. Carus, Arnold, Buchner, J. Müller, Langer, and many other prominent anatomists belonged, a school which attacked the problem of the segmental value of the cranial nerves by first determining perfectly independently the number of segments or skull-vertebre in the head, a determination made as a rule on very insufficient and often purely fanciful grounds, and having thus decided the number of segments, and therefore of segmental nerves, proceeding to apportion the several nerves to these segments, usually in a very arbitrary manner. The writers named above differ, indeed, in the number of head-segments they respectively adopt, but agree in the principle on which they work, viz., determining the number of segmental nerves Srom that of the supposed segments or vertebre composing the skull.

Stannius was the first to deal with the question in a more philosophical spirit, and to attempt to determine the number of segmental nerves by a direct study of the nerves themselves.

The results of his investigations! are contained in his invaluable treatise on the Peripheral Nervous System of Fishes published in 1849. He leaves the three nerves of special sense out of consideration for the same reason as Stieda and the other anatcmists we have mentioned, i.e, that they are rather parts of the brain than true nerves. He also omits the eye-muscle nerves, remarking that any attempt to homologise them with spinal nerves “encounters insuperable difficulties on account of their peculiar origin, their absence of ganglia, and their exclusive distribution to the muscles ,of a sensory apparatus, which are in no way comparable with the muscles of the vertebra.” The remaining nerves, however, Stannius deals with in a very complete and masterly manner. He considers that the fifth, seventh, ninth, and tenth nerves are each equivalent to a spinal nerve, and compares in detail both the roots of origin and the branches of these nerves with those of the spinal nerves.

Stannius was also the first to point out the very important relations of the ventral branches of these segmental cranial nerves to the visceral arches. In the essay quoted above he shows how each visceral arch is supplied by two branches belonging to different nerves, one running along its anterior border, and one along the posterior. He points out how the first branchial arch is supplied along its anterior border by the glosso-pharyngeal nerve, and along its posterior by the vagus; how the remaining branchial arches are supplied by the vagus, each arch by branches from separate stems; how the hyoid arch is supplied in front by the hyoidean branch of the facial nerve, and behind by the anterior branch of the glosso-pharyngeal ; how the mandibular arch has the mandibular branch of the trigeminal nerve along its anterior border, and along its posterior the anterior branch of the facial, which he identifies as the chorda tynpant of Aves and Mammalia ; and finally, how the upper jaw is supplied by the ophthalmic and maxillary divisions of the fifth nerve.

He concludes this portion of his treatise with the following very suggestive sentence : — * Hence it follows that the number of the ventral branches of each cranial nerve, and the number of the spinal-like (segmental) cranial nerves is not determined so much by the number of the skull-vertebre as by that of the visceral arches.”

In thus stating that the number of segmental cranial nerves was no longer to be determined by preconceived ideas concerning the composition of the skull, but by direct examination of the nerves themselves, Stannius rendered an invaluable service to morphology. Had he, indeed, gone one step further; had he been able to completely disabuse his mind of this notion of skull-vertebre which was exercising so pernicious an influence on the zoologists of the day, he would have anticipated by more than twenty years Gegenbaur’s announcement of that theory of the vertebrate skull which has since, with some slight modifications, been accepted almost universally.

While the school of morphologists we first dealt with determined the number of the segmental nerves by that of the skullseginents, Stannius showed conclusively that there was no relation whatever between the two, but that there was a very definite and remarkable one between the segmental nerves and the visceral arches. Gegenbaur went a step-further, and, starting with the segmental nerves and visceral arches, determined from them the number of head-segments, thus completely reversing the order of proceeding of the older school.

Gegenbaur is sometimes credited with being the first to establish the relations of the cranial nerves to the visceral arches, a determination which, as we have seen, had been already made by Stannius. The often quoted table of the cranial nerves given by Gegenbaur,’ contains, in fact, nothing that had not been already pointed out by Stannius, except an attempt to rank the labial cartilages as visceral arches, an attempt which has not met with general acceptance. Gegenbaur’s real merit consisted in pointing out that the ideal number of skull-vertebae, as determined by Oken and other “transcendental anatomists,” was to be left out of consideration altogether; that the evidence offered by the cranial nerves and visceral arches was to be accepted in full, and was to be taken as the basis for determining the number of segments in the head; and that the vagus nerve was, from the fact of its supplying more than one visceral cleft, to be considered as equivalent to more than one segmental nerve, and to be regarded as formed by the fusion of a certain number of primitively distinct nerves.

3 Gegenbaur, Joc. cit. p. 552.

Thus it has come to pass that the cranial nerves, while formerly considered of very subordinate importance, are now recognised as affording a very valuable and reliable clue to the solution of that favourite morphological problem—the segmentation of the vertebrate head ; and Gegenbaur’s paper, which was undoubtedly the chief means by which the cranial nerves were rescued from their former dependent position, must be viewed as marking a most important era in their history.

Attention being thus pointedly directed to the cranial nerves, their comparative anatomy and embryology quickly engaged the attention of zoologists ; and during the last five or six years our knowledge on these points has received very material additions, additions which have, on the whole, tended to strongly confirm Gegenbaur’s views, while causing modification of them in many secondary points.

The most important of these more recent contributions is undoubtedly the series of facts brought tu light by Balfour concerning the early stages of development of the spinal and cranial nerves in elasmobranch fishes. Balfour showed that, contrary to the generally accepted theory, the nerves are outgrowths from the cerebral nervous system, and therefore of epiblastic origin, instead of being, as formerly supposed, structures arising independently in the mesoblast and only acquiring a secondary connection with the brain and cord.

In the case of the spinal nerves, he showed that the two roots, anterior and posterior, arise separately and independently ; that the posterior roots are local outgrowths of a continuous longitudinal band — the neural crest — which grows out along the middorsal line of the spinal cord (fig. 1). By lateral growth of the dorsal summit of the cord the nerve roots of the two sides, which are at first (fig. 1) directly continuous with one another across the top of the cord, become separated to a certain extent (fig. 2). The nerve root on either side grows downwards, closely applied to the side of the cord, it then acquires a new or secondary attachment! to the side of the cord, some little distance below the primary one (fig. 3). A little later the primary attachment disappears, and the secondary alone remains as the permanent attachment of the posterior root to the cord (fig. 4).

The anterior roots arise later than the posterior, each as an independent conical outgrowth from the latero-ventral angle of the cord (fig. 3). The roots grow rapidly, and soon form elongated bands of fusiform cells, which retain their original points of origin from the cord. Each is at first, and for some time, quite distinct from the posterior root (fig. 3), with which, however, it subsequently unites to form the adult spinal nerve (fig. 4).

Further differences between the anterior and posterior roots are afforded by the fact that the posterior develops at a very early period a large ganglionic swelling—the future spinal ganglion—(figs. 3 and 4), while the anterior root is devoid of ganglion cells. The roots of origin of the anterior root are also very generally multiple, while those of the posterior roots, whether primary or secondary, are apparently invariably single.

Balfour’s observations were soon extended to birds and mammals, and the description given above is now recognised as that of the general and typical mode of development of the vertebrate spinal nerves. It was further found that the neural crest is not confined to the spinal cord, but extends forwards along the top of the brain, and that certain of the cranial nerves are developed from it in the same way as the posterior roots of the spinal nerves. By this discovery a new and very reliable clue to the segmental value of the cranial nerves is obtained, for it is clear that if certain of the cranial nerves do, and others do not, conform to the mode of development of the typically segmental spinal nerves, there is strong reason for regarding the former as being: of segmental value, and the latter as not.

Embryology has furnished us with one further test of the segmental value of cranial nerves, for which again we are indebted to Mr. Balfour, who bas shown that in elasmobranchs (and the observation has since been extended to other groups) the two halves of the ccelom or body-cavity at an early period extend forward on either side of the neck into the head, and that on the appearance of the visceral clefts each of these halves becomes cut up into a series of isolated compartments, one in each visceral arch If the visceral clefts and arches are segmental, it is clear that these “head-cavities,” as they are called, must be so also, and that they will therefure afford an additional clue to determining the segmental value of the nerves associated with them.

1 The account of this shifting is based on my own observations. Balfour expresses himself as ‘‘inclined to adopt this view” (Comparative Embryology, vol. ii. p. 872), but does not definitely do so.

Summary of Evidence of Segmental Value of Cranial Nerves

From what has been said above it will be evident that we have now several independent tests of the metameric or segmental value of the cranial nerves,—tests with all of which a nerve ought to comply to entitle it to rank as segmental. For convenience of reference, these tests, the majority of which have already been discussed, may be enumerated here : —

1. Segmental nerves develope at a very early stage as outgrowths from the neural ridge on the dorsal surface of the brain.
2. At an early period they shift downwards, and acquire new or secondary roots of attachment to the sides of the brain.
3. The general course of the main stem of a segmental nerve is at right angles, or nearly so, to the axis of the head at the point of origin of the nerve. This feature, which is explained more fully in the paper quoted above, is evident from an inspection of fig. 8,in which the directions of the segmental nerves are shown, and from the consideration that the course of segmental nerves must be approximately parallel to the boundaries of the segments to which they belong: a segmental nerve could not run transversely across a number of segments.
4. Segmental nerves have the characteristic relations to the visceral clefts and arches, and, therefore, also to the head-cavities in these arches, first pointed out by Stannius as noticed above, each nerve supplying the borders of one cleft, and therefore of two arches. Concerning this test, it may be noted that, although from the constancy of the relations of the visceral clefts to other structures in all vertebrates above Amphiorus, there can be no doubt that Gegenbaur, Huxley, Semper, and others are correct in maintaining the segmental value of these clefts, yet that the total absence of any correspondence between the visceral clefts and the body segments in Amphioxus, and still more in the Ascidians, makes it very doubtful whether this segmental character is a primitive one.

1 Balfour, Elasmobranch Fishes, pp. 206-209 ; also Marshall, ‘‘ Head-Cavities and Associated Nerves of Elasmobranchs,” Quart. Journ. of Micros. Science, January 1881.

2 Of. Marshall, ‘‘ The Morphology of the Vertebrate Olfactory Organ,” Quart. Journ. of Micros. Science, July 1879, p. 317.

3. Segmental nerves very constantly present ganglionic enlargements, either at or near their points of division into their two main ventral branches.

Having thus cleared the ground, and explained what we mean by a segmental nerve, and why it is of importance to determine which of the cranial nerves are of segmental value, and which are not, I propose to consider these nerves and discuss their claims in order, beginning with the most anterior ones, and taking them in the sequence usually adopted by anatomists,

I. The First or Olfactory Nerve

This nerve was until recently supposed, by reason of its development, to stand quite apart from the rest of the cranial nerves, and to be, properly speaking, a part of the brain rather than a nerve in the strict sense of the word.’ Instead of developing like the other nerves, the olfactory was stated to arise as a hollow outgrowth from the anterior part of the cerebral hemisphere—the so-called olfactory lobe or vesicle: it was also stated to arise considerably later than the posterior cranial nerves.

It is now known that these supposed distinctions between the olfactory and the other nerves do not really obtain,? but, on the contrary, that the olfactory nerves develope in precisely the same way as the other cranial nerves; that they arise at first from the upper part of the fore-brain and gradually shift downwards, acquiring by so doing a secondary connection with the

1 Vide, e.g., Huxley, Anatomy of Vertebrated Animals, p. 71; and Gegenbaur, Elements of Comparative Anatomy, English Translation, p. 515. 2 Marshall, ‘‘Morphology of Vertebrate Olfactory Organ,” Quart. Jowrn. of

Micros. Science, July 1879 ; and Balfour, Comparative Embryology, vol. ii. 1881, pp. 336 and 382.

cerebral hemispheres, of which they are at first completely independent; and, finally, that the olfactory lobe or vesicle so far from being the earliest part to be developed is actually the last; no vestige of it appearing in the chick until the seventh day of incubation, in the salmon till long after hatching, or in dogfish until stage O of Balfour's nomenclature.

If, then, the olfactory nerve agrees in all important features of its development with the other cranial, and the spinal nerves, the further question at once suggests itself—has it segmental value?! An examination of the evidence at our disposal, which is unfortunately far from complete, shows that there is much to be said in favour of such a view; thus, applying to the olfactory nerve the several tests of the metameric value of cranial nerves in the order given above, on p. 313, we obtain the following results :—

1. The olfactory nerve develops very early: the actual date of its first appearance is very difficult to determine, and has not yet been ascertained with certainty in any case, but in both the chick and the dogfish it appears at a very early stage of development, and in the chick, indeed, an attempt has been made to show that the olfactory nerve is “ one of the first nerves in the body to appear,” ? arising before any of the spinal nerves. There is also evidence, though as yet inconclusive, in favour of the origin of the olfactory nerve in the chick from the neural crest.

2. The olfactory nerve resembles the segmental nerves in undergoing during the earlier stages of its development a very considerable displacement of its root of attachment to the brain, and as this feature is one of the most remarkable characters of these segmental nerves, and is, so far as we know, confined to them, its occurrence in the olfactory nerve must be admitted to be of much weight.

In both the dogfish and chick the olfactory nerves are clearly recognisable before the cerebral hemispheres have commenced to develope, the nerves at this stage arising from the dorsal part of the sides of the original fore-brain or anterior cerebral vesicle.

1 I have dealt with this question at some length in a former paper on ‘‘The Morphology of the Vertebrate Olfactory Organ,” Quart. Journ. of Micros. Science, July 1879, to which I would beg to refer the reader who may desire further details than I can give here.

2 Marshall, ‘‘The Development of the Cranial Nerves in the Chick,” Quart. Journ. of Micros. Science, Jan. 1878, p. 23.

The hemispheres in the chick are lateral outgrowths of the forebrain, and are from the first situated above, or, on the dorsal side of the roots of the olfactory nerves; they grow forwards and upwards with great rapidity, driving the olfactory nerves down to the base of the brain, and so causing these nerves to appear to arise from their under and anterior part. Whether the root of the olfactory nerve undergoes any change comparable to the secondary attachment described above as occurring in the spinal nerves, has, however, not yet been ascertained.

3. The general course of the olfactory nerve in the early stages of development is, like the segmental nerves, at right angles to the axis of the head at the point of origin of the nerve, although, owing to cranial flexure, it is very far from being parallel to the hinder segmental nerves. This feature is shown in fig. 8,I. In the later stages of development, owing to the forward growth of the nasal region, this relation becomes completely lost,

4, Concerning the relations of the olfactory nerve to visceral arches and clefts, I must beg to refer the reader to the paper quoted above, in which I have drawn attention to “the very close resemblance as to form, structure, general relations, time of appearance, &c., existing between the olfactory organ and the gill clefts,” and have adduced other arguments on which I have attempted to establish the following conclusions :—“ That the olfactory organ is the most anterior visceral cleft; that the olfactory nerve is the segmental nerve supplying the two sides of that cleft in a manner precisely similar to that in which the hinder clefts are supplied by their respective nerves; and that the Schneiderian folds are homologues of gills.”?

5. The olfactory nerve is distinctly ganglionic near its root of origin from the brain in elasmobranchs and in the chick.

It would thus appear that although the evidence is at present far from conclusive, and although further information is needed on many points, notably concerning the earliest stages of development of the olfactory nerve, yet that the nerve answers fairly well to the tests of segmental value as defined above ; and it is important to note that the points in which it responds incompletely are precisely those on which our knowledge of the nerve is avowedly imperfect, and that in no case is a test directly contradicted. I am therefore disposed, while fully admitting the need for further investigation, to rank the olfactory nerve as the most anterior of the cranial segmental nerves, the nerve belonging to the first head-segment.

1 "Morphology of Vertebrate Olfactory Organ,” Quart. Journ. of Micros. Science, July 1879, p. 380.

The segmental value of the olfactory nerve has recently been advocated by Wiedersheim, who draws attention to the fact that in Epicrium, and probably in other Gymnophiona as well, there are on either side two olfactory nerves, one dorsal and one ventral, the roots of the two being perfectly independent, and some little distance apart. Wiedersheim considers that these two roots are homologues of the dorsal and ventral roots of a spinal nerve, and that by their discuvery the segmental rank of the olfactory nerve may be considered to be established.

A similar condition of the olfactory nerve in Pipa dorsigera has been figured, though not described, by Fischer.

These two cases, in both of which the additional root is the dorsal one, tend strongly to confirm the view taken above of the primitive connection of the olfactory nerve with the dorsal surface of the brain, and therefore presumably with the neural crest; but in the absence of any observations on either the development or the physiological properties of the two roots in question, I do not think that much weight can be attached to Wiedersheim’s suggestion of their homology with the roots of a spinal nerve.

Balfour argues against the segmental value of the olfactory nerve, on the ground that it is incompatible with the views which he holds concerning the primitive vertebrate mouth, and concerning the relations between the nervous systems of vertebrates and invertebrates. His views on these points are of very great interest and importance; but inasmuch as they involve the descent of Chetopods and Vertebrates, not from a common segmented ancestral type, but from a common unsegmented type, and also the existence of a group of segmented animals, which “ appears now to have perished” without leaving any trace behind, it would clearly be impossible to discuss them here in full. His theory that the vertebrate fore-brain is the homologue of the supra-cesophageal ganglia of Arthropods and Cheetopods is, however, to my mind open to very serious objections, some of the more weighty of which he has himself mentioned, viz. (1) that there is no actual anatomical or embryological break between the fore-brain and the hinder portion of the central nervous system, such as one might reasonably expect to find on his hypothesis; (2) that the lowest known vertebrate, Amphiovus, instead of lending any support to this view, distinctly contradicts it, the fore-brain being less differentiated from the hinder portion than in any other vertebrate, while “the termination of the notochord immediately behind the forebrain ”—almost the only direct evidence he adduces in favour of the “morphological distinctness” of the fore-brain—again fails completely, the notochord in Amphioxus, as is well known, extending to the extreme anterior end of the bead, some distance beyond the front end of the brain.

II. The Second or Optic Nerve

Although, as we have just seen, the statement that the olfactory nerve is rather a part of the brain than a nerve in the strict sense of the word is found on examination not to hold good, yet, as regards the optic nerve, it is certainly correct; the mode of development of the optic nerve, which is too well known to require a detailed description here, placing it in this respect in marked contrast to every other nerve in the body.

From the fore-brain or anterior cerebral vesicle two hollow lateral outgrowths arise—the optic vesicles. These become constricted at their origin from the brain, the constricted portions or optic stalks becoming ultimately the optic nerves. By a process of unequal growth of the different parts, coupled with a direct pushing in of the outer wall by the formation of the lens, each vesicle becomes doubled up on itself, the outer wall being pushed back into the inner, and so giving rise to the double-walled “ optic cup” or secondary optic vesicle.

This mode of development, which, with secondary modifications applies to all vertebrates except Amphioxus, and must therefore be considered as primitive so far as vertebrates are concerned, differs so fundamentally from the development of the hinder cranial or spinal nerves that no comparison whatever is possible between them. The optic nerve must therefore be regarded as one swi generis, and as one which can accordingly have no claim to be considered of segmental value.

The existence of this clearly non-segmental nerve between the olfactory and the hinder nerves is undoubtedly an objection to the view advocated above concerning the segmental value of the olfactory nerve; but until we obtain a clearer light than we are at present able to throw on the phylogenetic history of the vertebrate eye, and indeed of the vertebrate race altogether, it is difficult to gauge properly the weight of the objection.

The Eye-Muscle Nerves

Concerning the morphological value of these three nerves—the third, fourth, and sixth pairs— opinions have perhaps differed more than in the case of any of the other cranial nerves.

The nerves in question are small, with a singularly limited and constant distribution to the muscles moving the eyeball, and to certain other parts in connection with the eye, the third nerve supplying the rectus superior, rectus internus, rectus inferior, and obliqguus inferior muscles of the eyeball, also the levator palpebre superioris and the circular muscle of the iris; the fourth nerve supplying the odliguus superior muscle, and in many vertebrates sending sensory branches to the conjunctiva and the skin of the upper eyelid; and the sixth nerve supplying the rectus externus muscle, and in many forms the suspensory muscle of the bulb of the eye and the muscles of the nictitating membrane. In dealing with them it will be convenient to consider them at first collectively, inasmuch as many points of importance concern them all alike, and afterwards to consider briefly the several points of individual interest which they present respectively. ;

Until very recently it was the almost universal custom amongst anatomists, when discussing the segmental value of the cranial nerves, to exclude the eye-muscle nerves altogether from consideration, on the ground that they were not constant in their distribution, but that one or more of the muscles normally supplied by them might under special circumstances be supplied by branches of the fifth nerve, the further inference being drawn from these special cases that the eye-muscle nerves were primitively branches of the fifth nerve, which have in the majority of existing vertebrates attained independence and acquired the appearance of distinct nerves, a title to which they have really no claim.

This view has very recently indeed been advocated by Wiedersheim, whom I quote in order to illustrate my statements. In dealing with the fourth nerve in the frog he notices that it usually forms anastomotic communications with the ophthalmic branch of the fifth nerve as it crosses it, and that the number of these communicating branches is very variable. He then says :—“ Dies eben beschriebene Verhalten sowie auch dasjenige des Abducens und des spiter abzuhandelnden Oculomotorius liefert eine hiibsche Illustration zu der in héheren Thiergruppen in.immer starkerer Weise hervortretenden Tendenz der Augenmuskelnerven, sich von ihrem Stammboden, der Trigeminusgruppe, zu emancipiren, um endlich eine gut individualisirte Selbststandigkeit zu erlangen.”

As this view, so definitely expressed by Wiedersheim in the above passage, appears to have met with very general acceptance, and as it very seriously affects and concerns the subject of the present paper, I have taken some trouble to collect all the recorded cases in which the distribution of the eye-muscle nerves or the supply of the eye-muscles in vertebrates is said to present any constant deviation from the normal arrangement as noticed above; and I propose now to examine critically these alleged exceptions to the general rule.

1. Amphioxus — The azygos character of the eye and its extreme simplicity of structure render any comparison with the eyes of higher and more typical vertebrates perfectly futile.

2. Marsipobranchii.

(a) Hyperotreti.— Among the myxinoid fishes, according to Stannius, J. Müller Huxley Gegenbaur, and others, the eye muscle nerves are completely absent. Here again we are dealing with animals in which the eyes are in a very rudimentary condition, and the eye-muscles either absent or extremely imperfectly developed; so that, as pointed out by Schwalbe,> no importance can be attached to them in determining the question of the primitive independence of the eye-muscle nerves, and this consideration is much strengthened by the strong evidence we possess of the Myxinoids being degenerate or degraded forms.

1 Vide, e.g., Gegenbaur, ‘‘ Ueber die Kopfnerven von Hexanchus,” Jenaische Zeitschrift, 1871, pp. 548, 549; Huxley, Anatomy of Vertebrated Animals, 1871, p. 73; also Stieda and the various authors quoted by him in his ‘Studien ueber das centrale Nervensystem der Wirbelthiere,” Zeitschrift fir wissenschaftliche Zoologie, Bd. xx. 1870.

(0) Hyperoartii Attention has been directed to the condition of the eye-muscle nerves in the lampreys by a number of writers. According to Schlemm and d’Alton, the lampreys have independent eye-muscle nerves, but their number is diminished, and some of the muscles are supplied by the fifth nerve. The fourth nerve is described as having its usual origin behind the optic lobes and entering the orbit in company with the third, which has an independent origin in front of that of the fifth. The combined nerve, formed by the union of the third and fourth, divides into two main branches, an upper one supplying the rectus superior, and a lower one supplying the rectus internus and obliqguus superior. The three other muscles, viz. rectus inferior, rectus externus, and obliquus inferior, are said to receive their nerves from the trunk of the fifth nerve.

Fischer and Stieda also refer to the peculiar distribution of the eye-muscle nerves in the lampreys, but avowedly draw their information from Schlemm and D’Alton’s paper, from which it would appear that Huxley, and probably Owen and Güntheralso, derive their accounts.

5 Schwalbe, ‘‘Das Ganglion Oculomotorii,” Jenaische Zeitsehrift, Bd. xiii. . 71. p

6 Of. Balfour, Comparative Embryology, vol. ii. 1881, p. 268, note 2.

Gegenbaur! gives a slightly different account. He says that in Petromyzon there is an independent fourth nerve, but that the sixth is a branch of the fifth, which supplies the rectus inferior as well as the rectus externus, while the third nerve is limited in its distribution, supplying the rectus superior, rectus internus, and obliquus inferior. He gives no reference in support of his statement, and must therefore be supposed to make it on his own authority, especially as it differs notably from the accounts of all other writers whom I have been able to consult.

Concerning the above accounts, it appears that they can be reduced to two sources—(1) the description given in 1838 by Schlemm and D’Alton, which I have assumed to be the source from which Owen, Huxley, and Ginther obtain the accounts given in their text-books quoted above, because their descriptions, which are very brief, agree exactly with that of Schlemm and D’Alton, and add nothing to it; and (2) Gegenbaur’s description in 1871, which must be independent, inasmuch as it does not quite agree with Schlemm and D’Alton’s. According to Gegenbaur, the only peculiarity is that the sixth nerve is not independent but a branch of the fifth, which supplies the rectus inferior as well as the rectus externus ; while, according to Schlemm and D’ Alton, three of the muscles—the rectus inferior, rectus externus, and obliquus inferior—are supplied by the fifth nerve; and, in addition to this, the third and fourth nerves unite together, a point which Gegenbaur does not notice.

The dissection is a difficult one, on account of the small size of the nerves concerned; and additional evidence from direct observation is necessary before we can decide whether either of the above descriptions is perfectly correct.

There are, however, certain points of considerable importance which concern not only Petromyzon, but many other forms as well, and may be conveniently dealt with here.

Both the third and fourth nerves are distinctly stated to have independent roots of origin, and to arise from the normal situations in the brain; and this being the case, I wish to point out that the anatomical arrangement of the nerves would probably be more correctly described by saying that the third nerve, though having a separate root of origin, becomes connected with the fifth, so that in the adult some of its branches appear to be derived from the fifth; than by saying, with Huxley Stieda, and Giinther, that the muscles in question are supplied by branches of the fifth.

Fischer long ago adopted this view. He describes, on Schlemm and D’Alton’s authority, the condition of the nerves in Petromyzon in these words :—“ Genus Petromyzon duas Oculomotorii ostendit partes, alteram liberam, parisque quarti quoque continentem fibras, alteram cum Trigemino conjunctam;”! and Stannius gives still clearer expression to it; for after referring to Schlemm and D’Alton’s observations, he says:—‘“ Offenbar ist hier ein Theil der Wurzelelemente des N. oculorum motorius, so wie auch die Wurzel des N. abducens, in die Bahn des N. trigeminus, iibergetreten,” and remarks that it is quite possible that a very careful examination of the nerve-roots would show that the abducens has really an independent root of origin.

The point at issue is an important one, and must be clearly stated. When we find two nerves—the third and fifth, which in the great majority of vertebrates are independent of one another both in origin and distribution — in certain forms, as the lampreys, arising from the brain independently and normally, but becoming united together at some point or other of their course, so that it is no longer possible from mere anatomical observation to say with certainty to which of the two a given branch belongs, are we to infer, as is done tacitly or explicitly by many writers? that the condition shown by the lamprey is the more primitive one, and represents an intermediate stage in the process by which the eye-muscle nerves gradually emancipated themselves from their parent nerve—the fifth — and attained ultimately the complete independence they show in the great majority of existing vertebrates? Or, on the other hand, are we to infer that the independent origin of the third nerve is - primitive, and that its connection with the fifth, when, as in the lamprey, it does occur, is a secondarily acquired one?

1 Fischer, op. cit. p. 47, note 1.

3 Cf. the authors mentioned above, and especially the passage quoted from Wiedersheim on p. 320 above.

To my mind there can be no doubt whatever that the latter is the correct explanation ; and the chief reasons that lead me to think so are the following :-—

(a) Though we know of instances—notably in the case of the vagus—of nerves originally distinct and independent gradually becoming fused, and then this fusion getting thrown back to a very early developmental stage ; yet we know of no established case of a branch attaining independence, and acquiring the character of a distinct nerve.

(b) Supposing it were possible for such a process to occur, it would certainly be very surprising if, as in the supposed case of the third nerve, the process of differentiation should commence at the proximal end, and that there should be a stage in which the roots were independent and the two nerves still fused distally.

(c) There are very strong reasons; which we shall discuss later on, for viewing both the third and fifth nerves as segmental, and therefore primitively independent of one another.

(d) If Wiedersheim’s view were currect, we should certainly expect the third nerve of higher vertebrates in its early stages of development to show some indication of its supposed primitive connection with the fifth. So far, however, is this from being the case, that in all cases where the development of the third nerve has yet been traced, it is a perfectly independent nerve from the start.

(e) A crucial test is afforded by the fact that other nerves — eg. the fifth and seventh—though, as a rule, separate from one another throughout the vertebrate series, may in some forms become more or less closely united together, so that it is impossible by mere anatomical evidence to distinguish branches of the one from those of the other; the forms in which this fusion of the fifth and seventh nerves occurs being, as we shall see more fully later on, in many cases the same as those in which the fifth and the eye-muscle nerves tend to fuse. In the case of the dog-fish, in which this fusion of the fifth and seventh nerves is a marked feature of the adult state, all the stages of development are now known) and it is found that, so far from the state of fusion being a primitive one, the two nerves are in their early stages quite independent and some distance apart, as in other vertebrates, and that their subsequent gradual approximation and fusion are purely secondary characters.

1 Marshall, ‘‘On the Development of the Cranial Nerves in the Chick,” Quart. Journ. of Micros. Science, Jan. 1878, pp. 28-27 ; and ‘‘On the Head Cavities and Associated Nerves of Elasmobranchs,” Quart. Journ. of Micros. Science, Jan. 1881, pp. 78-83.

The above arguments appear to me to establish the proposition that the third nerve is primitively an independent one,” and that its partial fusion with the fifth, when it occurs, is a purely secondary and not a primary character.

If they prove the case for the third nerve, so also for the fourth and sixth nerves. The presence of independent roots of origin from the brain must be held to establish that, however close may be the connection- of their trunks with the fifth nerve, they are really independent nerves, and are not to be described as being “ replaced by branches of the fifth nerve.”

In the case of the lampreys, then, I hold that we have no reliable evidence of the third or fourth nerves being in any way abnormal in their distribution to the eye-muscles; while, as regards the sixth nerve, although no distinct root of origin has yet been seen, I hold, with Stannius, that a much more careful and searching investigation must be made for it before any statement as to its absence can be accepted.

3. Ganoidei — In the majority of ganoids the nerves of the eye-muscles have the normal arrangement, and are completely independent of the fifth, except where the third unites with the ophthalmic branch of the fifth at the ciliary ganglion. Only one exception is known.

In Lepidosteus, according to J. Müller, the arrangement is abnormal, the third and fourth nerves entering the orbit closely united with the ophthalmic division of the fifth, of which they appear as branches. The sixth nerve is described and figured as accompanying the main trunk of the fifth, but distinct from it.

1 Marshall and Spencer, “Observations on the Cranial Nerves of Scyllium,” Quart. Journ. of Micros. Science, July 1881, pp. 482-486.

2 The independence of the third nerve has recently been upheld on anatomical grounds by Schwalbe—Das Ganglion Oculomotorii ; and by Balfour, on embryological ones—Comparative Embryology, vol. ii.

3 J. Mũller, Ueber den Bau und die Grenzen der Ganoiden, 1846, p. 97, and plate iv. figs. 2 and 3.

Stieda, in his essay! before referred to, quotes Miiller’s account, but does so incorrectly, making Miiller say that there is a distinct fourth nerve, but that the third and sixth are replaced by branches of the fifth; whereas Miiller really says that the sixth is a distinct nerve, and that the third and fourth are not “replaced by branches of the fifth,” but contained in the ophthalmic nerve.

Stannius, referring to Mũller’s account, observes that it is probably merely another instance of juxtaposition of originally distinct nerves.

Concerning this alleged exception, we notice in the first case that it rests on a solitary description, which has not yet been confirmed, and that confirmation is needed is evident from the figures referred.to. Miiller gives two figures of the cranial nerves of Lepidosteus, which do not agree in all points with another ; indeed, the points of difference are so marked that the two figures are by no means easy to reconcile with one another. Miiller’s figure 3 appears to me to present nothing exceptional, except that the third and fourth nerves enter the orbit as one trunk, and that the fourth nerve at the point where it crosses the portio minor of the ramus ophthalmicus superficialis® is rather more extensively connected with this nerve than is usually the case. The nerve which Miiller marks y, and calls the “ophthalmic branch of the fifth” but which he does not seem to have followed to the brain, I see no reason for considering as other than what one would naturally suppose it to be from its distribution to all the eye-muscles except the rectus externus, 4.e., the combined third and fourth nerves. In Miiller’s figure 2 there is a remarkable point of difference, inasmuch as the nerve which I have considered in the former figure to be the proximal part of the portio minor, or trigeminal portion of the ramus ophthalmicus superficialis, is entirely omitted. No mention is made either in the text or in the description of the figures of this very important difference. I would further notice that, although the two figures in question are drawn of the same size and to the same scale, yet that the relative proportions of the several nerves, and more especially the extent to which they are fused with one another, are so very different in the two cases that one is driven to suppose either that the figures are taken from different specimens, in which case there must be considerable individual variability in the very points alleged to be exceptional, or else that one or other of the figures is taken from an incomplete dissection.

1 Stieda, loc. cit. p. 174.

2 Stannius, Das peripherische Nervensystem der Fische, p. 19.

3 For the nomenclature of these ophthalmic nerves, vide Marshall and Spencer, ‘© Observations on the Cranial Nerves of Scyllium,” part i, Quart. Journ. of Micros. Science, July 1881.

The above considerations lead to the conclusion that, in the absence of direct confirmation, Miiller’s account of the eyemuscle nerves in Lepidosteus does not prove that they are in any way exceptional, except in the fact of the third and fourth nerves entering the orbit as one trunk.

Very important information concerning these nerves in Lepidosteus has recently been afforded by Schwalbe, who finds, from a careful examination of the nerves and brain, that both the third and fourth nerves have independent origins from the brain ; a fact, which, as in the case of Petromyzon, must be held to conclusively prove that such connection as may actually occur between the fifth nerve on the one hand, and the third and fourth on the other, beyond their roots of origin,is of a purely secondary character, and that it does not in the very slightest degree militate against the claims of the third and fourth to rank as independent cranial nerves.

4, Teleostei.— The only recorded instances that I can find of deviation from the normal arrangement of the eye-muscle nerves among osseous fish are :-—

(a) Amblyopsis? the blind fish of the Mammoth cave of Kentucky, in which the eyes are rudimentary and functionless, and the eye-muscle nerves, as might be expected, absent.

(b) Stlurus glanis, in which, according to Stannius, the eyes are small, the eye-muscles very slender, and the eye-muscle nerves outside the skull closely united with the ophthalmic branch of the fifth. Stannius points out, however, that careful examination shows that all three nerves arise independently from the brain at the normal situations, and expressly notices that, but for the discovery of these extremely slender roots, the eyemuscle nerves of Silurus would have been beyond all doubt described as branches of the fifth nerve. It is of course probable that in the other species of blind fish, whether living in caves, as Typhlichthys, Stygicola. Gronias, Atlia, &c., or living at great ocean depths, as the Scopelide, the eye-muscle nerves are, as in Amblyopsis speleus, rudimentary or absent; but it will be sufficiently evident, from what has been already said, that neither these blind fish nor such cases as Silwrus tell in any way against the independent rank of the eye-muscle nerves.

2 Noticed by Stannius, Das peripherische Nervensystem, p. 18 ; and Schwalbe, loc. cit. p. 71.

5. Dipnoi.— In his account of the African Lepidosiren (Protopterus) annectens, Prof. Owen? notices that the optic nerves “are remarkably small, in correspondence with the feeblydeveloped organs of vision;” also that the eyeball “has no special muscles, whence the absence of the third, fourth, and fifth cerebral nerves.”

According to Hyrtl? in the South American form, Lepidosiren paradoxa, in which also the eyes are very small, the four recti muscles are present, but the two- obliqui not represented. The eye-muscle nerves were not found, but were believed to be replaced by two fine branches of the ophthalmic division of the fifth nerve, which branches, however, were not traced into the rectt muscles.

Prof. Humphry’s® description of Lepidosiren (Protopterus) annectens very closely agrees with Hyrtl’s of LZ. paradoxa in the points with which we are now concerned. He finds, contrary to Owen, that the four recti muscles “may clearly be distinguished,” though there are no obliqui. “Special nerves to these muscles (the third, fourth, and sixth) were not found ;” but the ophthalmic division of the fifth is described as giving off in the orbit “ciliary and oculo-motor nerves,” which, however, do not appear to have been traced to their distribution.

Gegenbaur‘* simply quotes Hyrtl to the effect that all three eye-muscle nerves are represented by branches of the fifth ; which, however, is a wider and more positive statement than Hyrtl really made.

' Owen, ‘Description of the Lepidosiren annectens,” Trans. Linnean Soc., vol. xviii, 1839, p. 340.

2 Hyrtl, “Lepidosiren paradoxa,” Prag. 1845, p. 44.

3 Humphry, Observations in Myology, 1872 ; The Muscles of Lepidosiren annec tens with the Cranial Nerves, pp. 77 and 79. 4 Gegenbaur, Hexanchus, p. 549.

Stannius also states, on Hyrtl’s authority, that the eyemuscle nerves have no independent roots ; and Huxley notes that in Lepidosiren “the three motor nerves of the eyeball are completely fused with the ophthalmic division of the fifth,” a condition which he is disposed to view as the most primitive arrangement met with among vertebrates.

In considering what importance is to be attached to this often-quoted exception to the general rule, we have first to notice that we are dealing with animals in which the eyes are “very small” and “feebly developed ;” secondly, that the eyemuscles are so small that their very existence was not only overlooked, but expressly denied, by so competent an anatomist as Prof. Owen; thirdly, that the two anatomists, Hyrtl and Humphry, who have described these muscles, agree in saying that the recti muscles are alone present, a condition clearly not fully realised by those who state, on Hyrtl’s authority, that the fourth nerve is, like the third and sixth, represented by a branch of the fifth; fourthly, that in neither of the cases mentioned were the nerves actually traced into the muscles in question.

To these points we must add one, urged with great force by Schwalbe, and which acquires much weight from the cases of Petromyzon and Lepidosteus already considered, viz., that a sufficiently careful examination of the brain has not been made to render us certain as to the alleged absence of independent roots of origin for such of the eye-muscle nerves as may be present.

The importance of Schwalbe’s warning is strikingly exemplified by the recent observations of Wiedersheim on the nervous system of Lepidosiren (Protopterus) annectens. Wiedersheim describes a moderately long but exceedingly slender nerve which leaves the skull through a special foramen in front of that of the fifth, and loses itself in the eye-muscles in a manner he was unable to determine with certainty. In spite, however, of taking “all conceivable pains,’ he was unable to ascertain whether this hitherto overlooked eye-muscle nerve arises independently from the brain, or is a mere branch of the fifth, though he is inclined himself to regard it as an independently arising third nerve.

Under these circumstances, and especially when we consider Wiedersheim’s discovery of a distinct eye-muscle nerve, and his statement of the extreme difficulty he experienced in tracing this nerve even to the limited extent which he succeeded in doing, we must, I think, conclude that, whatever subsequent investigation may tell us, Lepidosiren at present offers no definite or reliable evidence against the statement that the eye-muscle nerves are independently arising nerves in all vertebrates in which the eye-muscles themselves are present.

6. Amphibia.— Statements of exceptional innervation of one or more of the eye-muscles among Amphibia are by no means uncommon ; and though I have devoted some time to making my list as complete as possible, I am far from certain that I have succeeded in collecting all the alleged cases. The following list includes all I have been able to refer to, and certainly all that are mentioned in the standard works and papers on the subject :—

A. Apoda (Gymnophiona).— Wiedersheim, in his monograph on this group, mentions that in Cecilia the eye-muscles are present, but of exceedingly small size, so small indeed that he could not make out either their number or arrangement; neither was he able to ascertain anything concerning their innervation ; indeed, he makes no mention whatever of the eye-muscle nerves. Fischer also failed, from his dissection of a single specimen, to make out anything definite concerning the eye-muscle nerves. Inasmuch as the eyes of Cecilia are very small, it would seem probable that we have here another instance of rudimentary eyes, accompanied very possibly by reduction in the number of eyemuscles; and we have already seen that the evidence yielded by such cases cannot be accepted as in any way affecting the question of the primitive independence of the eye-muscle nerves.

B. Caudata (Urodela).

(a) Proteus.— The specimen of Proteus dissected by Fischer was, like that of Cwcilia, too imperfectly preserved to permit him to make any positive statement concerning the eyemuscle nerves; indeed, he calls attention to and expressly regrets his inability to determine whether these nerves are present or absent. The eyes of this cave-dwelling amphibian are situated beneath the skin, and are of very rudimentary structure, being arrested at what is in other vertebrates a very early embryonic condition.2 As has been pointed out by Schwalbe,? Fischer does not in any way deny the existence of eye-muscle nerves, but merely records his inability to find them in a very imperfectly preserved specimen.

(0) Salamandra and Triton.—I take these two genera somewhat out of their proper zoological order, because they afford perhaps the most widely-known and frequently-quoted examples of abnormal innervation of the eye-muscles—instances which must accordingly be carefully considered.

Fischer, who was the first to draw attention to the point, states that in Salamandra and Triton the third nerve, though rising independently from the brain, only supplies three of the eye-muscles—the rectus internus, rectus inferior, obliquus inferior —the rectus superior receiving a special branch from the “ nasal division” of the fifth, which branch is absent in Anura in which the innervation is normal. In discussing the importance of this, he says:—“ Quid igitur veri possit esse similius, quam quod partium duarum, in quas penes Salamandrina divisum sit oculomotorius, altera eandem, quam in Ecaudatis retinuerit formam, altera cum Trigemino se conjunxerit?” The fourth nerve in the same two genera, according to Fischer, “seems to have coalesced with the fifth pair;” at any rate, he was unable to discover any independent nerve, and the obliquus superior muscle is supplied by the “nasal branch” of the fifth. The sixth nerve is perfectly normal both in its origin and distribution; it passes very close to the Gasserian ganglion, but is really distinct from it, and leaves the skull by an aperture distinct from that of the fifth.

? For a description and figure of the eye of Proteus, vide Semper, Animal Life, International Science Series, pp. 78, 79.

3 Schwalbe, Das Ganglion Oculomotorii, p. 72.

Fischer, op. cit. pp. 24, 25, 32, and 47.

Fischer’s careful descriptions, which have the great advantage of being illustrated by as careful figures, have been referred to by many writers—Stannius,? Gegenbaur,? Hoffmann,* Stieda,® &c.—who, however, have added nothing to our knowledge on the subject from direct observations of their own.

Schwalbe,® who appears to be the only anatomist since Fischer’s time who has directly investigated this interesting point, has furnished additional information of great value concerning it. He finds, in confirmation of Fischer's statement, that the nerve to the rectus superior muscle is derived, not from the third nerve, but from the “nasal branch” of the fifth; but points out that before this nerve is given off the third and nasal nerves cross and lie in very close contact with one another. He considers it probable that at this point there is direct connection between the two, although he was unable to prove it; and he accordingly supports the view, held also by Fischer and Stannius, that the supply of the rectus superior by the fifth is only apparent and due to the close connection and partial fusion of the third and fifth nerves at this point of crossing.

Concerning the fourth nerve, Schwalbe’s results are more positive, and of great importance. He finds that although in the majority of specimens of Salamandra maculosa he dissected the arrangement described by Fischer obtained, the nerve to the obliquus superior appearing as a branch of the nasal nerve, yet that in some cases, one of which he figures,’ the fourth may be a completely independent nerve, arising from the brain in the normal position.

Reviewing, then, these much-quoted cases of Salamandra and Triton, we find that Fischer’s account of the anatomical arrangement of the nerve is confirmed by Schwalbe. We find that the sixth nerve is perfectly independent both at its root and along its whole course—is, in fact, in every way normal. That the fourth nerve is, as a rule, an apparent branch of the “nasal branch” of the fifth, but, at least in Salamandra, may be not uncommonly an independent nerve, normal in every respect. That the third nerve always arises independently from the brain ; that it crosses the “nasal branch” of the fifth, lying in cloye contact. with it as it does so; and that it supplies only three muscles—the rectus internus, rectus inferior, and obliquus inferior —the rectus superior receiving its branch from the “nasal nerve,” and this branch coming off beyond the point of crossing of the third and nasal nerves; and that this condition of things is interpreted by both the writers, who have investigated it directly— Fischer and Schwalbe—as merely implying that the third nerve has become partially fused with the fifth.

1 Fischer, op. cit., tab. ii. fig. 2 (Salamandra), and fig. 3 (Triton). 2 Stannius, Das peripherische Nervensystem, p. 19.

3 Gegenbaur, Hexanchus, p. 549, note 1.

4 Hoffmann, Bronn’s Thierreich, Bd. vi. heft. ii. Amphibia, p. 204. 5 Stieda, loc. cit. p. 174.

6 Schwalbe, Das Ganglion Oculomotorit, pp. 25-27.

7 Schwalbe, Das Ganglion Oculomotorii, Tab. xiii. fig. 13.

Concerning this “nasal nerve,” from which, in the two genera in question, the branch to the rectus superior always, and that to the obliquus superior usually, arises, there is a further point of importance. Schwalbe? has attempted to prove that this “nasal nerve” really corresponds, in part at least, to the ramus ophthalmicus profundus of Selachians. The point could only be decided by a study of the development of this nerve in Urodela, of which at present we know nothing; but should Schwalbe prove to be correct, the, very slight amount of deviation from the normal condition which we have found to be all that really occurs in Salamandra and Triton would be still further reduced; for embryology teaches us that the ramus ophthalmicus profundus of Selachians is really a connecting branch between the third and fifth nerves, which cannot be said to belong distinctly to either one or the other, and that the portion of this nerve beyond the point at which it crosses the third nerve, from which portion we have seen that the branch to the rectus superior arises, has nothing whatever to do with the fifth, but belongs really to the third nerve.” .

From what has been said above, I think that no other conclusion can be drawn than that the cases of Salamandra and Triton do not afford any reason for regarding the eye-muscle nerves as other than independent and constant nerves.

1 Schwalbe, Das Ganglion Oculomotorii, p. 26.

2 Marshall, ‘‘ Head Cavities and Associated Nerves of Elasmobranchs,” Quart. Journ. of Micros. Science, January 1881, p. 89; and Marshall and Spencer, “Cranial Nerves of Scyllium,” Quart. Journ. of Micros. Science, July 1881, pp. 494 seq.

(c) Menobranchus.— Gegenbaur! states, on Fischer’s authority, that in Menobranchus, as in Salamandra and Triton, the fourth nerve is replaced by a branch of the fifth. I have been unable to refer to Fischer’s account, so that any discussion of the case would be unprofitable. It is, however, very possible that the condition is really what Schwalbe has shown to occur in Salamandra.

(d) Siredon.— Fischer? has established that the third and fourth nerves are normal in origin and distribution, but was unable to make out anything definite concerning the sixth nerve.

(e) Cryptobranchus.—Schmidt, Goddard, and V. d. Hoeven are quoted by Hoffmann ® as stating that in the Cryptobranch the third and fourth are independent nerves, but that the sixth is a branch of the nasal division of the fifth.

Professor Humphry‘ remarks that the dissection of the cranial nerves is difficult, on account of the “ tough areolar tissue of the animal and the numerous accompanying veins.” He was unable to “discover the third, fourth, or sixth nerves in the orbit.” The third and fourth were, however, found in the cranial cavity, but not the sixth.

Here, again, our information is too imperfect to allow definite conclusions to be drawn. If the sixth nerve really appears as a branch of the fifth, it is of importance to note that, as is evident from Professor Humphry’s figure, the fifth and seventh nerves are quite distinct from one another—a point to which we shall refer when considering the Anura.

C. Anura.—tThe condition of the eye-muscle nerves in Anura has been carefully investigated by a number of anatomists, notably by Fischer ® and Schwalbe. The results of these investigations are as follows :—In all Anuwra that have been examined, the third and fourth are distinct and independent nerves, with normal origin and distribution. In Pelobates and Bombinator the third leaves the skull by the same foramen as the fifth, with which it is in very close contact, though the two nerves are really distinct.

1 Gegenbaur, Hexanchus, p. 549, note 1.

2 Fischer, Anatomische Abhandlungen iiber die Perennibranchiaten und Derotremen, Hamburg, 1864, p. 127.

3 Bronn’s Thierreich, Bd. vi.

4 Humphry, Observations in Myology, p. 45, and pl. iv. fig. 22.

5 Fischer, Amphibiorum nudorum Neurologic, specimen primum, pp. 8-22 and 45-48. ,

6 Schwalbe, Das Ganglion Oculomotorti, pp. 28-31.

The sixth nerve in all cases has an independent origin from the brain in the normal position. In Bufo, the sixth nerve preserves its independence along its whole course, and is in all respects perfectly normal. In the other Anura examined—viz., Pipa, Rana, Pelobates, Bombinator, and Hyla—the sixth nerve, though arising independently, unites with the Gasserian ganglion, and the branch to the rectus externus is derived from the “ nasal branch” of the fifth.?

But little criticism is called for by the above account. As was urged in the case of Lepidosiren, the presence of a distinct root of origin in the normal position must be held to prove that the sixth nerve is in the cases quoted above really an independent nerve, in spite of its apparent fusion with the fifth at the Gasserian ganglion. The fact that the sixth in an allied genus (Bufo) retains its independence, is an additional argument in favour of the fusion being secondarily acquired ; and this view must be considered to be established by the statement made by Stannius,? on Fischer’s authority, that the sixth nerve is independent of the fifth in the larval stages of those forms which, - when adult, have the two nerves fused.

This concludes the list of recorded instances of exceptional innervation of the eye-muscles. Leaving out, as we are fairly entitled to, the cases of Amphioxus and of those forms in which, as in Amblyopsis, the eyes are rudimentary and functionless; the results of an examination of the remaining instances may be stated thus :—

1 Fischer, op. cit. p. 5, and tab. ii. fig. 1.

2 Of. Fischer, op. cit. pp. 8-22, and tab. i. fig. 2 (Hyla) fig. 8 (Bombinator), fig. 4 (Pelobates); and tab. ii. fig. 1 (Pipa), fig. 4 (Rana); also Wyman, Anatomy of the Nervous System of Rana pipens, New York, 1853, pp. 26-28; also Wiedersheim in Ecker’s Anatomie des Frosches, Zweite Abtheilung, 1881, pp. 20-21.

% Stannius, Handbuch der Zootomie, Zweites Buch, Die Amphibien, 1856, p. 150, note 3.

1. That in no single instance has it been established that any one of the eye-muscle nerves is replaced by a branch of the fifth, or of any other nerve—the cases in which this is alleged to occur being far more naturally explained by supposing partial fusion between the nerves concerned to have occurred.

2. That in the alleged cases of replacement of one or more of the eye-muscle nerves by a branch of the fifth nerve, the “branch of the fifth” in question is very probably the ramus ophthalmicus profundus, which is really a communicating nerve between the third and fifth, belonging as much to one as to the other in its posterior portion, and in its anterior part belonging exclusively to the third. .

3. That the instances in which the absence of one or other of the eye-muscle nerves has been alleged are either, as in Petromyzon, Lepidosteus, Pipa, Hyla, &c., cases in which the nerves in question arise from the brain in a perfectly normal manner, and after running a certain distance within the skull become connected more or less intimately with the fifth nerve; or else cases in which, as in Lepidosiren, the eyes are small, the eye-muscles imperfectly developed, and the descriptions of their anatomy incomplete and unsatisfactory.

4, That such cases do not in any way invalidate the proposition that the third, fourth, and sixth are independent nerves throughout the vertebrate sub-kingdom.

I propose now to consider briefly the leading features exhibited by the eye-muscle nerves individually.

III. The Third, or Oculomotor Nerve

Since the third nerve is found to be an independent nerve throughout the vertebrate series, it becomes of interest to inquire whether or not it possesses segmental value.

Observations by different investigators during the last few years have tended very strongly to support, if, indeed, they may not be said to have established, the claim of the third nerve to rank among segmental nerves. Inasmuch as this point has been very fully discussed recently’ I do not propose to go over the whole of the evidence here, but shall merely apply, in a somewhat summary manner, the several tests of segmental value in the order given on a previous page.

• 1 Marshall, ‘ Development of Cranial Nerves in Chick,” Quart. Journ. of Micros. Science, January 1878, pp. 23-27 ; and ‘‘ Head Cavities and Associated Nerves of Elasmobranchs,” Quart. Journ. of Micros. Science, January 1881, pp. 78-83 ; also Schwalbe, Das Ganglion Oculomotorit.

1. Though the earliest stages of development of the third nerve have not yet been ascertained with precision in any case, yet there is very strong reason for thinking that in the chick, at any rate, the third nerve develops, like the hinder cranial nerves and the posterior roots of the spinal nerves, as ar outgrowth from the neural crest on the top of the mid-brain.?

2. Inasmuch as, at a rather later, though still early period— about the sixtieth hour in the chick, and stage K of Balfour's nomenclature in the dog-fish—the third nerves arise from the base of the mid-brain, very near the mid-ventral line, it is clear that, if the observations on the earlier stages are correct, the roots must shift downwards at an early period, and to an extent unequalled by any other nerve.

Kolliker has described. the later stages of this shifting, as seen in rabbit embryos, as follows:?—In an embryo 12 days 5 hours old, and 7 mm. long, the third nerve arose from the mid-brain, not from its ventral surface, but about half-way up its side; later on it shifts ventralwards, “like the ganglionated cranial nerves and the sensory spinal roots,” being found on the ventral surface of the mid-brain in an embryo of the 14th day, and 15 mm. long.

3. The course of the main stem of the nerve is (fig. 8, IV.) at right angles to the axis of the head at the point of origin of the nerve.

4. Morphologists are very far from agreeing as to the existence of a visceral cleft in front of the mouth, so that it would be premature to discuss the relations of the third nerve to this “lachrymal cleft,” for whose existence there is, however, much to be said. Concerning the head cavities, however, the evidence yielded by the third nerve is of a perfectly detinite and convincing character. The nerve in Elasmobranchs passes downwards and backwards from its root of origin to the interval between the dorsal ends of the first and second head-cavities, where it expands into a ganglionic swelling—the ciliary ganglion. Beyond this point the main trunk of the nerve passes down between the two cavities, the relations of the third nerve to the first and second cavities being precisely the same as those of the fifth nerve to the second and third cavities

1 Supra, p. 318.

2 Of. Balfour, Comparative Embryology, vol. ii. p. 379.

3 Kolliker, Entwicklungsgeschichte des Menschen und der hiheren Vhiere Zweite Auflage, 1879, p. 613.

5. As just noticed, there is a very evident ganglionic swelling at the point of division of the third nerve into its two main branches.

These considerations are, I think, when taken in conjunction with its previously established constancy throughout the vertebrate series, sufficient to establish the proposition that the third nerve is of segmental nature. The further question, whether the third represents an entire segmental nerve, or only a portion of one, will be best answered by considering the fourth nerve.

IV. The Fourth or Trochlear Nerve

Having established the constancy of this nerve, we have now to consider its morphological import. Concerning its development we know very little, but that little is of importance. In the dog-fish it has been shown? that the fourth nerve, at the earliest period at which it has been recognised, arises from the brain at the same spot as in the adult, i.e, the dorsal surface of the hinder end of the mid-brain ; further, that its course is from the first that of a segmental nerve.

Now, if the visceral clefts and arches, and the head cavities give us, as they most certainly do, reliable clues as to the segmentation of the head, then it is seen at once that there is no room for a segmental nerve between the third and fifth nerves ; and therefore, if the fourth is of segmental nature, it must belong to one or other of these nerves.

The following considerations seem to point very strongly to the third and fourth nerves being connected together, and favour the view that they are together equivalent to a segmental nerve.

1, The two nerves in question, the third and fourth, both arise from the mid-brain or middle cerebral vesicle. Furthermore, they are the only nerves that arise from this division of the brain, either in the embryo or the adult. There are independent reasons for thinking that these brain-vesicles have segmental value ;1 and though these reasons may not be considered conclusive on the point, they nevertheless lend some support to the view that the two nerves arising from one of these vesicles belong to the same segment.

• 1 Marshall, ‘*‘ Head Cavities and Associated Nerves of Elasmobranchs,” Quart. Journ. of Micros. Science, Jan. 1881, pp. 78 seq.
• 2 Marshall and Spencer, ‘‘ Cranial Nerves of Scyllium,” Quart. Journ. of Micros, Science, July 1881, pp. 672-674.

2. The third and fourth nerves, though arising separately from the brain, may be connected together more or less intimately beyond their roots of origin. This, for instance, is a marked feature both in Petromyzon and Lepidosteus, also in Salamandra and Triton, if Schwalbe is correct in identifying the “ nasal branch” of the fifth with which both the third and fourth nerves are connected as the ramus ophthalmvicus profundus.

3. According to Meynert,? the third and fourth nerves arise in the adult from a common nucleus. This has, however, been denied by Forel,’ though supported by other investigators, and probably requires confirmation.

4. The fourth, though chiefly known as a motor nerve, is really in many animals a nerve of mixed function, giving off in Selachians and Amphibians* sensory branches to the conjunctiva and skin of the upper eyelid. This point is of importance, because if the third and fourth are together eqivalent to a segmental nerve, it would be only reasonable to expect that certain of its fibres should be sensory; and analogy would certainly lead us to look for sensory branches in the portion with the more dorsally situated root, ze, the fourth nerve, which, as we have just seen, does actually present such sensory fibres.

5. That the fourth nerve is itself not an entire segmental nerve is rendered probable by the fact, noticed by Schwalbe, that it has no ganglion, and is strongly supported by the further fact that the third nerve almost certainly arises at first from the dorsal surface of the brain, and beyond all doubt is, during its early stages, attached much higher up the side of the brain than it is at a later stage, ze, that the third nerve behaves like a posterior spinal root.

1 Vide Foster and Balfour, Elements of Embryology, part i. p. 188; and Marshall, Development of Nerves in Birds, this Journal, vol. xi. p. 510.

2 Meynert, ‘‘The Brain of Mammals,” Stricker’s Histology, New Sydenham Society’s Translation, vol. ii. pp. 444, 445.

3 Forel, Haubenregionen.

4 Schwalbe, Das Ganglion Oculomotorii, p. 14 ; Wiedersheim, Morphologische Studien, p. 21; and in Ecker’s Anatomie des Frosches, p. 24; also Hoffmann, Bronn’s Thierreich, Bd. vi. p. 208.

Since, as we have seen, there is no room for a separate segmental nerve between the third and the fifth, I am inclined to view the third and fourth nerves as together equivalent to a segmental nerve, which has divided into two portions, whereof one —the fourth—has remained in its primitive position on the top of the brain, while the other—the third—has, like the other cranial nerves and the posterior spinal roots, shifted downwards, the extent of the shifting being greater than that of any of the other nerves, but the several steps of the process probably the same as in these. This view will be found to be very closely in accordance with that advocated by Schwalbe.1

V. The Fifth or Trigeminal Nerve

It will be convenient to continue the consideration of the cranial nerves in the usual sequence, and to take the remaining eye-muscle nerve—the sixth—after the trigeminal.

The fifth nerve completely fulfils all the conditions of a true segmental nerve.? It appears very early as an outgrowth from the neural crest. The root of origin from the brain shifts down at an early period, acquires a secondary attachment to the side of the brain, and loses its primary attachment completely. The direction of the main stem is at right angles to the axis of the head at the point of origin of the nerve. The maxillary and mandibular branches are related to the maxillo-mandibular or buceal cleft in the manner characteristic of the posterior segmental nerves, as was first pointed our by Stannius, The relations of the fifth nerve to the second and third head-cavities are of a perfectly typical nature; and finally a ganglionic enlargement—the Gasserian ganglion—is present in the nerve a short distance above its division into the two main branches.

1 Schwalbe, Das Ganglion Oculomotorii, pp. 77, 78.

2 For the development of the fifth nerve in Elasmobranchs, vide Balfour, Elasmobranch Fishes, 1878, p. 196-198; also Marshall and Spencer, ‘‘ Observations on the Cranial Nerves of Scyllium,” Quart. Journ. of Micros. Science, July 1881, pp. 474-479 ; in the Chick, wide Marshall, Quart. Journ. of Micros. Science, Jan. 1878, pp. 28-32; and in the Rabbit, Kolliker, Hntwicklungsgeschichte, 1879, pp. 610-712.

The only possible doubt as to the independent segmental value of the fifth nerve hinges on the fact that in the two lower classes of vertebrates— Pisces and Amphibia—the fifth is very generally fused more or less completely with the seventh in the adult condition; the fusion sometimes, as in most fishes, involving the roots to a greater or less extent, sometimes, as usually in Amphibians, occurring a short distance beyond the roots and close to the Gasserian ganglion.

This approximation or fusion of the fifth and seventh nerves has, as mentioned above, been employed by J. Miller, Stieda, and others, as an argument against the two nerves being of independent segmental value.

A crucial test of the force of this argument is afforded by a study of the development of the roots of the two nerves in Elasmobranchs, in which the fusion of the roots in the adult is so complete that what is really one of the roots of the seventh has hitherto been almost invariably described by anatomists as a root of the fifth. In the dog-fish it has been shown that the two nerves, though so intimately connected in the adult, are in the early embryonic stages perfectly distinct from one another, and some distance apart, as far from one another, indeed, as they are in corresponding stages of such forms as the chick or lizard in. which they remain completely separate throughout life; and that the gradual approximation and fusion of the two nerves, which occur during the later developmental stages, all the steps of which have been traced, must, like the partial fusion which we have seen may occur in some forms between the third and fifth nerves, be viewed as purely secondary features.

In early stages of both Teleosteans and Amphibians, I have also noticed that the roots of the fifth and seventh nerves are perfectly distinct from one another, and some distance apart, and that their subsequent approximation must accordingly be, as in Elasmobranchs, of a purely secondary nature.

1 A full account of the development of the roots of the fifth and seventh nerves in the dog-fish, and of the relation of the embryonic to the adult roots, will be found in the paper by Mr. Spencer and myself quoted above, Quart. Journ. of Micros, Science, July 1881, pp. 482-486.

The claim of the fifth nerve to rank as an independent segmental nerve must, I think, from what has been said above, be considered as definitely established.

VI. The Sixth or Abducént Nerve

The proper morphological position of this nerve is by no means easy to determine with any degree of certainty ; and the views of different writers on the point are far from being in harmony with one another.

In a former section of this paper we have established the fact that the sixth is an independent nerve throughout the vertebrate sub-kingdom. It always supplies the rectus externus muscle of the eyeball, and may supply other parts as well; thus, in reptiles it supplies the retractor muscle of the bulb of the eye, and in Batrachia the suspensor muscle of the bulb and the muscles of the nictitating membrane! Jn all cases it as a purely motor nerve. Indeed, if we omit the eleventh and twelfth pairs, which are not constant cranial nerves, the sixth is not only the most purely motor cranial nerve, but the only exclusively motor one throughout the vertebrate series.

Its point of origin from the brain in adult vertebrates is also a remarkable and constant one. It arises from the under surface of the medulla, very close to the mid-ventral line, and vertically below, or more usually slightly posterior to the common root of origin of the seventh and eighth nerves. In some cases the root may be in front of that of the seventh nerve. The root is always slender, and devoid of ganglion cells.

Concerning the development of the sixth nerve, we unfortunately know but little. At the fifth day in the chick? and ata corresponding stage in the dog-fish, it has been detected and described, its appearance and relations being practically identical in the two cases. It is a slender nerve, with no ganglion cells at any point in its length, arising from the ventral surface of the hind-brain, below the seventh nerve, by a number of small slender roots, and running forward to the rectus externus muscle, in which itends. The roots are from the earliest period at which the nerve can be recognised close to the median ventral line (fig. 7, VI.), and some distance below the root of the seventh (fig. 7, VII.), from which they are From the start perfectly distinct. So far as can be inferred from negative evidence, the sixth nerve appears to develope later than the seventh and other segmental nerves.

1 Stannius, Handbuch der Zootomie, Zweite Auflage, Zootomie der Amphibien, 1856, p. 150.

2 Marshall, ‘‘ Development of Cranial Nerves of Chick,” Quart. Journ. of Micros. Science, Jan. 1878, pp. 23-25.

3 Marshall, ‘‘ Head Cavities and Associated Nerves of Elasmobranchs,” Quart. Journ. of Micros. Science, Jan. 1881, pp. 89-93.

From the above account it is clear that the sixth has no claim whatever to segmental rank, inasmuch as it distinctly fails to answer to any one of the tests of such rank laid down on page 313. It does not develope from the neural crest. The roots of origin do not shift downwards, but are from their first appearance in the adult position. The course of the nerve is nearly parallel to, and certainly not perpendicular to the axis of the head. It has not the definite relations to the visceral clefts and arches, and to the head cavities, characteristic of a segmental nerve. And it has no ganglion cells at any point in its length.

As the nerve is not an independent segmental nerve, it must either belong to one of the segmental nerves or else be a nerve of altogether exceptional nature. The latter supposition should, I think, only be adopted as a last resource if all the other attempts at explanation fail, and I therefore propose now to consider the relations of the sixth to the segmental nerves, or rather to the fifth and seventh nerves, which are clearly the only ones which could claim it.

By the majority of writers who have discussed this point, the sixth is referred to the fifth. Thus, Gegenbaur considers the sixth to be an independently arising motor root of the fifth, a view which Schwalbe! also adopts. Wiedersheim? speaks of the fifth and sixth nerves as together making up a segmental nerve; while Huxley? is disposed to view the sixth as primarily part of the fifth.

Notwithstanding the weight of authority against me, I think that the sixth nerve should be grouped with the seventh, and not with the fifth, for the following reasons :—

1 Schwalbe, Das Ganglion Oculomotorii, p. 74.

2 Wiedersheim, Morpholigische Studien, p. 23. 3 Huxley, Anatomy of Vertebrated Animals, p. 73, note | 344 DR. A. MILNES MARSHALL.

1. Tn the early stages of both chick and dog-fish the roots of the sixth are completely behind those of the fifth nerve. Indeed, the majority of the roots are even behind the roots of the seventh; and although a transverse section may, as in fig. 7, pass through the roots of both sixth and seventh nerves, yet the root of the sixth in such a section is the most anterior of the series, the other roots being further back, and completely behind the seventh root.

2. In adult vertebrates, also the sixth nerve usually arises beneath or slightly behind the seventh, very rarely in front of it.

3. Though the sixth nerve may, beyond its root, be closely connected with the fifth, yet it is important to notice that all the cases—Petromyzon, Lepidosiren, Pipa, Rana, and other Anura —in which it ts described as fusing with the fifth, are also cases im which the seventh and fifth nerves are very closely connected together, so that the connection between the sixth and fifth in these instances by no means proves that the sixth belongs to the fifth, but is more probably due to the same cause—whatever it may be—that determines the approximation or fusion of the seventh and fifth nerves.

Concerning the actual value of the sixth nerve, I see no reason to alter the opinion I have previously expressed, that the sixth nerve may be regarded as having the same relation to the seventh that the anterior root of a spinal nerve has to its posterior root. I shall return to this point when considering the seventh nerve.

VII. The Seventh or Facial Nerve

As to the segmental value of the seventh nerve there can be no doubt whatever ; for, like the fifth, it completely and indisputably fulfils all the conditions of a segmental nerve laid down on page 313.

It develops very early as an outgrowth from the neural crest on the dorsal surface of the hind-brain (fig. 5); at an early stage the nerve acquires a new or secondary attachment to the side of the brain (fig. 6); but, unlike all the other nerves, cranial or spinal, the original or primary root is retained as well as the secondary root ; whereas in all the other nerves the primary attachment appears to be lost (figs. 3 and 4). The general course of the nerve is at right angles to the axis of the head at its point of origin; the relation of its branches to the hyomandibular cleft, first pointed out by Stannius, and afterwards insisted on by Gegenbaur, are those of a typical segmental nerve, as are its relations to the head cavities; whilst, finally, it is ganglionic at its division into the two main ventral branches.

• 1 For an account of the development of the seventh nerve in Elasmobranchs, vide Balfour, Elasmobranch Fishes, 1878, pp. 198-202 ; and Marshall and Spencer, Quart. Journ, Micros. Science, July 1881, pp. 679-691 ; in the Chick, vide Marshall, Quart. Journ. Micros. Science, Jan. 1878, pp. 34-36 ; and in Mammals, Kolliker, Entwicklungsgeschichte.

As to the independent rank of the seventh nerve, I have already discussed fully the theory that the seventh and fifth nerves are connected together primarily, and have stated the arguments leading to the conclusion, that although in many vertebrates—fishes and amphibians—the two nerves are more or less closely fused together, yet that embryology shows that this fusion is a secondarily acquired character.

The relation between the sixth and seventh nerves is of still greater importance, from its bearing on the disputed question of whether there are to be found in any of the cranial nerves roots strictly comparable with the anterior roots of the spinal nerves.

In dealing with this question, it is first necessary to establish certain general conclusions concerning the cranio-spinal nerves. As was first pointed out by Balfour, the posterior roots of the spinal nerves must be regarded as of a more primitive nature than the anterior roots, the grounds on which this conclusion is based being the following :—

1. The actual mode of development of the two kinds of roots in the spinal nerves. As noticed in a previous page, the posterior roots appear before the anterior ones, and are also in their mode of development of a more primitive character than these latter, the posterior roots consisting at first entirely of undifferentiated spherical or polygonal cells, while the anterior roots are almost from their first appearance fibrillar.

2. The condition of the nervous system in Amphioxus, in which, as conclusively shown by Balfour, all the nerves arise by single roots, which roots correspond to the dorsal or posterior roots of other vertebrates, and which must clearly in Amphioxus be of mixed motor and sensory function.

• 1 Supra, p 312. * Balfour, Elasmobranch Fishes, p. 193.

From these facts the further conclusion is drawn “ that primitively the cranio-spinal nerves of vertebrates were nerves of mixed function with one root only, and that root a dorsal one ; and that the present anterior or ventral root is a secondary acquisition.” !

Concerning the several steps by which these anterior roots have been acquired, the evidence at our disposal is of an imperfect, and in great part merely conjectural character. Still I think that, though we may not be able to solve the problem completely, we can at any rate define its limits fairly accurately, and perhaps indicate the path along which the solution will ultimately be found.

The problem is how, from animals resembling Amphiowus in possessing only dorsal roots to the nerves, and these dorsal roots consequently of mixed function, has the type of spinal nerve met with among existing vertebrates, with two distinct roots, dorsal or sensory and ventral or motor, been derived.ref>Balfour, Elasmobranch Fishes, p. 198.</ref>

It appears to me that there are two ways in which we can conceive this change as having come about :—

Firstly, we might suppose that in some way, and for some reason, the sensory and motor portions of the originally single root became completely separated from one another, and that while the sensory portion of the nerve retained the primitive mode of development and position of attachment of the root, the motor portion acquired a new mode of development and a new position of attachment, and then united farther on with the posterior root to form a spinal nerve. - On this view the motor and sensory roots of a spinal nerve correspond to the motor and sensory portions of the single root of Amphioxus.

Or, secondly, we might imagine the anterior root to be, not the motor portion of the original root, but an altogether new development, an independent outgrowth from the spinal cord to supply the more complicated system of muscles that would necessarily accompany the gradual perfection and complication of the internal skeleton; that this new root was at first completely independent of the original or dorsal root, and for a time coexisted with a dorsal root of mixed function ; that in the case of the spinal nerves the whole motor function gradually got transferred to, or usurped by, the new root; while the two roots, originally separate along their whole length, became united to form the mixed trunk of the spinal nerve.

Now, although there are very considerable and obvious difficulties in the way of accepting either of these alternatives, yet it appears to me that the second is far more in accordance with the actual facts than the first, and that it offers a ready explanation of many points unintelligible on the first hypothesis. Thus, the second view explains why in actual development the anterior spinal roots appear later than the posterior, and why they are for some time quite distinct from these latter; it also explains such cases as Petromyzon, in which the anterior and posterior roots of the spinal nerves are said to remain distinct from one another throughout life.

By far the most important argument, however, in favour of the second hypothesis is afforded by the explanation it yields of the condition of the cranial nerves as compared with the spinal; and in connection with this point I would direct special attention to the statements already made concerning the sixth and seventh nerves.

It has been shown above that the seventh nerve in Elasmo branchs develops in a manner precisely similar to the posterior roots of the spinal nerves; that it arises as an outgrowth from the neural crest (figs. 5, VII.), the nerves of the two sides being at first directly and widely continuous with one another across the top of the brain; that by growth of the mid-dorsal | roof of the brain the two nerves get separated from one another (figs. 6, VII.) ; that the root acquires a secondary attachment to the side of the brain (figs. 7, VII.), but that, unlike the other cranial or the spinal nerves, it retains the primary as well as the secondary root throughout life. In this respect the seventh is, with the possible exception of the fourth, the most primitive nerve in the body, inasmuch as it exists throughout life in a condition which is only a transitory one in all the other nerves. However unexpected this point may be, I cannot but think that it is one of the greatest importance in the determination of any question concerning the morphology of the cranial and spinal nerves.

The seventh being a very primitive nerve, there is strong a priori reason for thinking that the sixth nerve, which we have seen reason for grouping with the seventh, is also of a primitive nature, and it is clear that on the second hypothesis such is the case, the complete independence of the sixth nerve being merely the retention of a primitive character, while its limited and special distribution to muscles not present in Amphioxus affords a very possible explanation of its appearance in higher vertebrates. On the first hypothesis, on the other hand, the sixth nerve would be, not a root which had retained its primitive independence of the seventh, but a root which had as a perfectly exceptional occurrence acquired independence, a view directly contradicted by the primitive condition of the seventh itself.

It must surely be regarded as a very significant fact that a transverse section through the hind-brain of either an embryo or adult Klasmobranch passing through the roots of the sixth and seventh nerves (fig. 7) agrees absolutely in all essential points with a section at an early embryonic stage through the roots of a spinal nerve in the same animal (fig. 3), ae, that a condition which is transitory in the case of the spinal nerves is permanently retained in the case of the sixth and seventh nerves. This fact, which is the strongest possible argument in favour of the second hypothesis, clearly directly contradicts the first.

If the doctrine that the cranial nerves are more primitive than the spinal appear at first sight paradoxical,! I would point out that there is independent evidence in favour of the head retaining a more primitive condition than the body. Thus the skull, though subjected to very extensive secondary modifications, is really in a more primitive state than the vertebral column, for the skull represents the permanent retention of a condition, that of a continuous unsegmented cartilaginous tube, which is only transitory in the case of the vertebral column except in the lowest vertebrates ; the division of the cartilaginous tube into segments or vertebrae never occurring, and in all probability never having occurred in the skull, though so constantly present in the vertebral column. The fact that it is in the lowest vertebrates alone that this unsegmented condition is retained in the trunk as well as in the head, is a strong argument in favour of the view that the head is really in a more primitive condition than the trunk as regards skeletal elements.

• I have myself on a former occasion both felt and urged this objection (‘‘ Head Cavities of Elasmobranchs,” Quart. Journ. of Micros. Science, Jan. 1881, p. 91). Further investigation has convinced me that I was then wrong, and that Balfour was right in considering (Elasmobranch Fishes, p. 193) the cranial nerves as more primitive than the spinal, though I do not agree with his conclusion that the cranial nerves have no anterior roots.

On the second hypothesis, the mixed—motor and sensory— nature of the seventh nerve is explained as due, like the persistence of the primary root and the independence of the sixth nerve, to retention of the primitive condition, and the extreme variability presented by the relative importance of the sensory and motor functions of the seventh nerve in different vertebrates may help to render intelligible how the posterior spinal roots, which were originally of mixed function, have become converted into purely sensory roots.

If the hypothesis advanced above should prove correct, it would be only reasonable to expect that the posterior roots of the spinal nerves should in some exceptional cases be found to retain in part their primitive mixed character, and to coexist as mixed posterior roots with exclusively motor anterior roots. I am not aware of any such cases, or of the existence of any residual physiological phenomena that would support such a view, but would suggest that a direct investigation of the functions of the spinal roots in the lampreys, where the two roots are stated to remain distinct from one another throughout life, might conceivably lead to interesting results.

The application of the hypothesis to the remaining cranial nerves is sufficiently obvious from the accounts given of them. The main point of difficulty concerns the determination of the presence or absence of anterior motor roots to these nerves; and on this point I have no additional evidence beyond what I have already stated elsewhere.”

VIII. The Eighth or Auditory Nerve

In all the forms in which the development of the auditory nerve has been ascer 1 The following quotation from Balfour, which I only became acquainted with after the above passage was written, strongly confirms this view :—‘‘ This development (of the skull) probably indicates that the basilar plate contains in itself the same elements as those from which the neural arches and the centra of the vertebral column are formed, but that it never passes beyond the unsegmented stage at first characteristic of the vertebral column.”

—Comparative Embryology, vol. ii. p. 467.

2 Marshall, ‘‘ Head Cavities and Associated Nerves of Elasmobranchs,” Quart. Journ. of Micros. Science, Jan. 1881, pp. 91-93.

tained, it arises as part of the seventh nerve. Neither its development nor its anatomical relations afford the slightest ground for thinking it to be of segmental rank.?

IX. The Ninth or Glosso-pharyngeal Nerve

Like the auditory, the ninth nerve can be disposed of very briefly, but for a directly opposite reason. Since Gegenbaur confirmed Stannius’ account of its relations to the first branchial cleft, the claim of the glosso-pharyngeal to rank as an independent segmental nerve has been very generally admitted; and as the history of its development? shows that it conforms in all respects to the characters of a segmental nerve as defined on page 313, it would be superfluous to discuss in detail its now universally recognised claims to segmental value.

X. The Tenth or Vagus Nerve

The tenth nerve stands in much the same position as the ninth, with the exception that while the glosso-pharyngeal is a single segmental nerve, the vagus, from its relations to a number of visceral clefts, must be considered as equivalent to an equal number of segmental nerves fused together. This was first pointed out by Stannius, and subsequently developed in much more detail by Gegenbaur ; and since the publication by the latter of his memorable essay on the cranial nerves of Hexanchus, has been accepted almost universally as the true theory of the morphological value of the tenth nerve. It is only necessary to add here that the study of its development shows that it completely fulfils all the conditions required of segmental nerves.

Concerning the number of primitively separate segmental nerves fused together to form the vagus, we cannot speak positively. The greatest number of clefts supplied by it in vertebrates above Amphiozus is met with among the Marsipobranchit and in Notidanus, where it supplies the six posterior branchial clefts, and must therefore be equivalent to at least six segmental nerves.

1 For the development of this nerve in Elasmobranchs, vide Balfour, Elasmobranch Fishes, p. 198; in the Chick, Marshall, ‘‘ Development of Cranial Nerves in Chick,” Quart. Journ. of Micros. Science, Jan. 1878, pp. 34-36.

2 For the development of the gloss-pharyngeal and vagus nerves in Elasmo branchs, vide Balfour, Elasmobranch Fishes, pp. 202, seg.; in the Chick, Marshall, loc cit. pp. 86-89.

Whether this is the full number, however, is a point not yet decided.

XI. and XII. The Eleventh or Spinal Accessory, and Twelfth or Hypoglossal Nerves

Neither of these nerves is constant as a cranial nerve throughout the vertebrate series, a fact which renders it very doubtful whether the claim of either of them to segmental value could be entertained. For this reason, and partly because I am at present engaged in investigating their development, about which we know as yet very little, I do not propose to deal further with them in the present paper. Forming, as they do, the connecting links between cranial and spinal nerves, they may be expected to yield valuable evidence concerning the validity of the hypothesis propounded above concerning the relations between these two groups of nerves.

Summary

The conclusions arrived at concerning the segmental value of the cranial nerves may be expressed in a tabular form thus :—

Segment. Nerve. Visceral Cleft. | Visceral Arch. 1. Preoral. I. Olfactory. Olfactory. III. Oculomotor, 2 De. i IV. Trochlear. Lachrymal. Maxillary. 3. Oral. V. Trigeminal. Buccal. 7 : Mandibular. VII. Facial, Spiracular or . 4, Postoral. VI. Abducent. yomandibular. Hyoid. 5. Do. IX. Glosso-pharyngeal.| 1st Branchial. 1st Branchial. 6. Do. X. Vagus, 1st branch.} 2nd ” 2nd ” 7 Do. » 2nd ,, 3rd. ” 8rd ” 8 Do. » 8rd ,, 4th * 4th ” 9. Do. » 4th ,, 5th ” 5th ” 10. Do. » Sth ,, 6th ” 6th ” 11. Do. » 6th ,, 7th

Bibliography

List of chief Works and Papers referred to, arranged

1838. 1839.

1840. 1843. 1844, 1845. 1846,

1849.

1851. 1855. 1856.

1864.

1866. 1870.

1871.

1872.

1875.

1877. 1878.

1879.

1880. 1881.

according to date of publication.

ScuLEmN v. p’Atton.—Ueber das Nervensystem der Petromyzon. Miiller’s Archiv., p. 262.

Owen.—Description: of the Lepidosiren annectens. Trans. Linnean Society, vol. xviii.

J. Mt.uer.—Vergleich. Neurologie d. Myxinoiden.

Fiscuer.—Amphibiorum nudorum Neurologie specimen primum.

J. Mtuier.— Handbuch der Physiologie des Menschen.

Hyrri.—Lepidosiren paradoxa.

J. Mttizr.— Ueber den Bau und die Grenzen der Ganoiden.

Strannius.—Das peripherische Nervensystem der Fische.

ARNOLD.—Handbuch der Anatomie des Menschen.

Wrman.—Anatomy of the Nervous System of Rana pipiens.

Srannius.—Handbuch der Anatomie der Wirbelthiere. Zweite Aufluge.

FiscHer.—Die Gehirnnerven der Saurier.

OwEn.—Anatomy of Vertebrates, vol. i. Srrepa.—Studien iiber des centrale Nervensystem der Wirbelthiere. Zeitschrift f. wissenschaftliche, Zoologie, Bd. xx. GxrGENBaUR.—Ueber die Kopfnerven von Hexanchus u. ihr Verhaltniss zur Wirbeltheorie d. Schadels. Jenaische Zeitschrift, Bd. vi.

Huxiey.—Manual of the Anatomy of Vertebrated Animals,

Meynert.—The Brain of Mammals. Stricker’s Histology, vol. ii, New Sydenham Society’s Translation.

Houmpury.—Observations in Myology.

Batrour.—On the Development of the Spinal Nerves in Elasmobranch Fishes. Phil. Trans, vol. cxxxvi.

MarsHatit.—On the early Stages of Development of the Nerves in Birds. Journal of Anatomy and Physiology, vol. xi.

Batrour.—Monograph on the Development of HEilasmobranch Fishes.

GEcENBAUR.— Elements of Comparative Anatomy, English Translation.

Marsuatt.—The Development of the Cranial Nerves in the Chick. Quart. Journ. of Micros. Science, vol. xviii.

Kouiiker.—Entwicklungsgeschichte des Menschen und der hcheren Thiere. Zweite Auflage.

MarsHatt.—The Morphology of the Vertebrate Olfactory Organ. Quart. Journ. of Micros. Science, vol. xix.

ScuwaLBe.—Das Ganglion Oculomotorii. Jenaische Zeitschrift, Bad. xiii.

Wiepersuetm.— Die Anatomie der Gymnophionen.

GutntHeEr.— Introduction to the Study of Fishes.

WieversHeim.—Morphologische Studien, Heft. i.

Batrour.—Treatise on Comparative Embryology, vol. ii. THE SEGMENTAL VALUE OF THE CRANIAL NERVES. 353

1881. Marsnaurt.—On the Head Cavities and Associated Nerves of Elasmobranchs. Quart. Journ. of Micros. Science, vol. xxi. MarsHatu and Spencer.—Observations on the Cranial Nerves of Scyllium. Quart. Journ. of Micros. Science, vol. xxi. WirpersHEIM.—Die Anatomie des Frosches, von Dr. Alexander Ecker. Zweite Abtheilung.

Description oF Plate X.

illustrating Dr. Marshall’s Paper on the Segmental Value of the Cranial Nerves.

Alphabetical List of References.

a.r. Anterior root of a spinal nerve. B. Buccal or mouth cleft. Br.1. First branchial cleft. Br.2. Second brancial cleft. Br.3. Third branchial cleft. Br.4, Fourth branchial cleft. Cc. Cerebellum. g. Ganglion on posterior root of spinal nerve. m.b, Mid-brain. mp. Muscle plate. n. Notochord. NV.c. Neural crest. Olf. Olfactory pit or cleft. p.r. Posterior root of a spinal nerve. Sp. Spiracular or hyomandibular cleft. S.a. Primary attachment of posterior root of spinal nerve. 4.8. Secondary attachment of posterior root of spinal nerve. 2. Second head-cavity. 3. Third head-cavity. I. Olfactory nerve. III. Oculomotor nerve. IV. Root of fourth or trochlear nerve. V. Trigeminal nerve. _ V.0. Maxillary branch of trigeminal nerve. VI. Abducent nerve. VII. Facial nerve. : VIId. Buccal branch of facial nerve. VIIa. Primary root of attachment of facial nerve. | VII. Secondary root of attachment of facial nerve. VIII. Auditory nerve. IX. Glosso-pharyngeal nerve, X. Vagus nerve.

Figs. 1 to 4 illustrate the chief stages in the development of the spinal nerves, as shown by transverse sections through the spinal cord ; they are copied, with some modifications, from figures given by Balfour in his paper on “The Development of the Spinal Nerves in Elasmobranch Fishes,” published in vol. cxxxvi. of the Philosophical Trunsactions.

Fig. 1 shows the posterior roots arising as outgrowths from the neural crest on the summit of the spinal cord. Stage I.

Fig. 2 shows the shifting outwards of the primary attachment of the posterior root, caused by lateral growth of the mid-dorsal portion of the cord ; also the first rudiment of the anterior spinal root on one side. Stage between I and K.

Fig. 3 shows the thinning of the primary root, S.a., and the acquiring of the secondary root of attachment, S.B., to the side of the cord some way below the primary root. In Balfour's figure this secondary attachment is not so clearly shown as in the figure given here. Ihave, from a direct investigation of the point, satisfied myself that this figure and the account given in the text represent correctly the process as actually occurring in Elasmobranchs.

Fig. 4 shows the definite acquirement by the posterior root of its secondary or permanent attachment, S.B., the primary root having lost all connection with the cord, and being represented solely by the portion of nerve projecting above the secondary root. Shows also the anterior root more fully developed, and on the right connected with the posterior to form a complete spinal nerve. Stage K. This figure differs from Balfour’s (plate xvii. I. 1) (1) in showing the posterior root on both sides instead of on the right side only ; (2) in showing both anterior and posterior roots in the same section, to do which the section must be supposed to be not perfectly transverse, but somewhat oblique, as the anterior roots are not directly beneath the posterior, but a short way in front of them.

Figs. 5 to 7 illustrate the several stages in the development of the seventh and sixth cranial nerves of Elasmobranchs, as shown by a series of transverse sections through the mid-brain and roots of these two nerves at different ages. They are copied from figures of my own, illustrating a paper by Mr. Spencer and myself, on “The Cranial Nerves of Scyllium,” Quart. Journ. of Micros. Science, July 1881.

Fig. 5 shows the primary root of attachment, VIIa., of the seventh nerve to the top of the mid-brain. The stage figured is intermediate between the stages in the development of the spinal nerve represented in figs. 1 and 2. Stages between I and K.

Fig. 6 shows the acquirement of the secondary root of attachment, VIIZ., to the side of the hind-brain, the primary root, VIIa., still persisting : owing to the growth of the dorsal surface of the brain the primary roots of the two sides are now widely separate. Stage K.

Fig. 7 shows the persistence of both primary and secondary roots of attachment of the seventh, and the appearance of the sixth nerve at a position and in a manner identical with those of the anterior spinal roots. As in fig. 4, the section is a somewhat oblique one, as the sixth is not vertically below the seventh, but slightly posterior to it. Stage N.

Fig. 8. A diagrammatic view of the head of a young vertebrate embryo from the left side, showing the several segmental nerves and their relations to the visceral clefts. Only 4 branchial clefts have been represented ; the hinder ones would be precisely similar to the others, and would, like the second, third, and fourth, be applied each by a branch of the vagus nerve.

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