(1) That the front part of the lateral line is undoubtedly supplied by branches which arise in the ordinary way from the intestinal branch of the vagus; and we should not expect to find part of the lateral line supplied by nerves which originate in one way, and the remainder supplied by a nerve having a completely different and abnormal mode of origin.
(2) The growth of the lateral line is quite independent of that of the lateral nerve: the latter arises subsequently to the lateral line, and, so far as is shewn by the inconclusive observation of my earliest stage, as an offshoot from the intestinal branch of the vagus; and though it grows along at first in close contact with the lateral line, yet it never presents, so far as I have seen, any indubitable indication of becoming split off from this, or of fusing with it.
(3) The fact that the cranial representatives of the lateral line are supplied with nerves which originate in the normal way[232], affords a strong argument in favour of the lateral line receiving an ordinary nerve-supply.
Considering all these facts, I am led to the conclusionthat the lateral nerve in Elasmobranchii arises as a branch of the vagus, and not as a direct product of the external epiblast.
An interesting feature about the lateral line and the similar cephalic structures, is the fact of these being the only sense-organs in Elasmobranchii which originate entirely from the mucous layer of the epiblast. This, coupled with the well-known facts about the Amphibian epiblast, and the fact that themucous canals are the only sense-organs which originate subsequently to the distinct differentiation of the epiblast into mucous and horny layers, goes far to prove[233]that the mucous layer is to be regarded as the active layer of the epiblast, and that after this has become differentiated, an organ formed from the epiblast is always a product of it.
Muscle-plates.
The muscle-plates at the close of stage K were flattened angular bodies with the apex directed forwards, their ventral edge being opposite the segmental duct, and their dorsal edge on a level with the middle of the spinal cord. They were composed of two layers, formed for the most part of columnar cells, but a small part of their splanchnic layer opposite the notochord had already become differentiated into longitudinal muscles.
During stage L the growth of these plates is very rapid, and their upper ends extend to the summit of the neural canal, and their lower ones nearly meet in the median ventral line. The original band of muscles (Pl.11, fig. 8,m.p´), whose growth was so slow during stages I and K, now increases with great rapidity, and forms the nucleus of the whole voluntary muscular system. It extends upwards and downwards by the continuous conversion of fresh cells of the splanchnic layer into muscle-cells. At the same time it grows rapidly in thickness, but it requires some little patience and care to unravel the details of this growth; and it will be necessary to enter on a slight digression as to the relations of the muscle-plates to the surrounding connective tissue.
As the muscle-plates grow dorsalwards and ventralwards their ends dive into the general connective tissue, whose origin has already been described (Pl.13, fig. 1). At the same time the connective-tissue cells, which by this process become situated between the ends of the muscle-plates and the skin, grow upwards and downwards, and gradually form a complete layer separating the muscle-plates from the skin. The cells formingthe ends of the muscle-plates retain unaltered their primitive undifferentiated character, and the separation between them and the surrounding connective-tissue cells is very marked. This however ceases to be the case in the parts of the muscle-plates on a level with the notochord and lower part of the medullary canal; the thinnest sections and most careful examination are needed to elucidate the changes taking place in this region. The cells which form the somatic layer of the muscle-plates then begin to elongate and become converted into muscle-cells, at the same time that they are increasing in number to meet the rapid demands upon them. One result of these changes is the loss of the original clearness in the external boundary between the muscle-plates and the adjoining connective-tissue cells, which is only in exceptional cases to be seen so distinctly as it may be inPl.13, figs. 1 and 8. Longitudinal horizontal sections are the most instructive for studying the growth of the muscles, but transverse sections are also needed. The interpretation of the transverse ones is however rendered difficult, both by rapid alterations in the thickness of the connective-tissue layer between the skin and the muscle-plates (shewn inPl.13, fig. 8), and by the angular shape of the muscle-plates themselves.
A careful study of both longitudinal and transverse sections has enabled me to satisfy myself of the fact that the cells of the somatic layer of the protovertebræ, equally with the cells of the splanchnic layer, are converted into muscle-cells, and some of these are represented in the act of undergoing this conversion inPl.13, fig. 8; but the difficulty of distinguishing the outline of the somatic layer of the muscle-plates, at the time its cells become converted into muscle-cells, renders it very difficult to determine whether any cells of this layer join the surrounding connective tissue. General considerations certainly lead me to think that they do not; but my observations do not definitely settle the point.
From these facts it is clear, as was briefly stated in the last chapter,that both layers of the muscle-plate are concerned in forming the great lateral muscle, though the splanchnic layer is converted into muscles very much sooner than the somatic[234].
The remainder of the history of the muscle-plates presents no points of special interest.
Till the close of stage L, the muscle-plates are not distinctly divided into dorsal and ventral segments, but this division, which is so characteristic of the adult, commences to manifest itself during stage M, and is quite completed in the succeeding stage. It is effected by the appearance, nearly opposite the lateral line, of a layer of connective tissue which divides the muscles on each side into a dorso-lateral and ventro-lateral section. Even during stage O the ends of the muscle-plates are formed of undifferentiated columnar cells. The peculiar outlines of the intermuscular septa gradually appear during the later stages of development, causing the well-known appearances of the muscles in transverse sections, but require no special notice here.
With reference to the histological features of the development of the muscle-fibres, I have not pushed my investigations very far. The primitive cells present the ordinary division, well known since Remak, into a striated portion and a non-striated portion, and in the latter a nucleus is to be seen which soon undergoes division and gives rise to several nuclei in the non-striated part, while the striated part of each cell becomes divided up into a number of fibrillæ. I have not however determined what exact relation the original cells hold to the eventual primitive bundles, or anything with reference to the development of the sarcolemma.
The Muscles of the Limbs.—These are formed during stage O coincidently with the cartilaginous skeleton, in the form of two bands of longitudinal fibres on the dorsal and ventral surfaces of the limbs. Dr Kleinenberg first called my attention to the fact that he had proved the limb-muscles inLacertato be derived from the muscle-plates. This I at first believed did not hold good for Elasmobranchii, but have since determined that it does so. Between stages K and L the muscle-plates grow downwards as far as the limbs and then turn outwards and grow into them(Pl.18, fig. 1). Small portions of several muscle-plates come in this way to be situated in the limbs, and are very soon segmented off from the remainder of the muscle-plates. The portions of muscle-plates thus introduced into the limbs soon lose their original distinctness, and can no longer be recognized in stage L. There can however be but little doubt that they supply the tissue for the muscles of the limbs. The muscle-plates themselves after giving off these buds to the limbs grow downwards, and by stage L cease to shew any trace of what has occurred (Pl.13, fig. 1). This fact, coupled with the late development of the muscles of the limbs (stage O), caused me to fall into my original error.
The Vertebral Column and Notochord.
In the previous chapter (p.325) an account was given of the origin of the tissue destined to form the vertebral bodies; it merely remains to describe the changes undergone by this in becoming converted into the permanent vertebræ.
This subject has already been dealt with by a considerable number of anatomists, and my investigations coincide in the main with the results of my predecessors. Especially the researches of Gegenbaur[235]may be singled out as containing the pith of the whole subject, and my results, while agreeing in all but minor points with his, do not supplement them to any very great extent. I cannot do more than confirm Götte's[236]account of the development of the hæmal arches, and may add that Cartier[237]has given a good account of the later development of the centra. Under the circumstances it has not appeared to me to be worth while recording with great detail my investigations; but I hope to be able to give a somewhat more complete history of the whole subject than has appeared in any single previous memoir.
At their first appearance the cells destined to form the permanent vertebræ present the same segmentation as the muscle-plates.This segmentation soon disappears, and between stages K and L the tissue of the vertebral column forms a continuous investment of the notochord which cannot be distinguished from the adjoining connective tissue. Immediately surrounding the notochord a layer formed of a single row of cells may be observed, which is not however very distinctly marked[238].
During the stage L there appear four special concentrations of mesoblastic tissue adjoining the notochord, two of them dorsal and two of them ventral. They are not segmented, and form four ridges seated on the sides of the notochord. They are united with each other by a delicate layer of tissue, and constitute the rudiments of the neural and hæmal arches. In longitudinal sections of stage L special concentrated wedge-shaped masses of tissue are to be seen between the muscle-plates, which must not be confused with these rudiments. Immediately around the notochord the delicate investment of cells previously mentioned, is still present.
The rudiments of the arches increase in size and distinctness in the succeeding stages, and by stage N have unquestionably assumed the constitution of embryonic cartilage. In the meantime there has appeared surrounding the sheath of the notochord a well-marked layer of tissue which stains deeply with hæmatoxylin, and with the highest power may be observed to contain flattened nuclei. It is barely thicker than the adjoining sheath, but is nevertheless the rudiment of the vertebral bodies.Pl.13, fig. 9,vb. Whence does this layer arise? To this question I cannot give a quite satisfactory answer. It is natural to conclude that it is derived from the previously existing mesoblastic investment of the notochord, but in the case of the vertebral column I have not been able to prove this. Observations on the base of the brain afford fairly conclusive evidence that the homologous tissue present there has this origin. Gegenbaur apparently answers the question of the origin of this layer in the way suggested above, and gives a figure in support of his conclusion (Pl.XXII.fig. 3)[239].
The layer of tissue which forms the vertebral bodies rapidly increases in thickness, and very soon, at a somewhat earlier period than represented in Gegenbaur'sPl.XXII.fig. 4, a distinct membrane (Kölliker's Membrana Elastica Externa) may easily be recognized surrounding it and separating it from the adjoining tissue of the arches. Gegenbaur's figure gives an excellent representation of the appearance of this layer at the period under consideration. It is formed of a homogeneous basis containing elongated concentrically arranged nuclei, and constitutes a uniform unsegmented investment for the notochord (videPl.13, fig. 10).
The neural and hæmal arches now either cease altogether to be united with each other by a layer of embryonic cartilage, or else the layer uniting them is so delicate that it cannot be recognized as true cartilage. They have moreover by stage P undergone a series of important changes. The tissue of the neural arches does not any longer form a continuous sheet, but is divided into (1) a series of arches encircling the spinal cord, and (2) a basal portion resting on the cartilaginous sheath of the notochord. There are two arches to each muscle-plate, one continuous with the basal portion of the arch-tissue and forming the true arch, which springs opposite the centre of a vertebral body, and the second not so continuous, which forms what is usually known as the intercalated piece. Between every pair of true arches the two roots of a single spinal nerve pass out. The anterior root passes out in front of an intercalated piece and the posterior behind it[240].
The basal portion of the arch-tissue likewise undergoes differentiation into a vertebral part continuous with the true arch and formed of hyaline cartilage, and an intervertebral segment formed of a more fibrous tissue.
The hæmal arches, like the neural arches, become divided into a layer of tissue adjoining the cartilaginous sheath of the notochord, and processes springing out from this opposite thecentres of the vertebræ. These processes throughout the region of the trunk in front of the anus pass into the space between the dorsal and ventral muscles, and are to be regarded as rudiments of ribs. The tissue with which they are continuous, which is exactly equivalent to the tissue from which the neural arches originate, is not truly a part of the rib. In the tail, behind the anus and kidneys, the cardinal veins fuse to form an unpaired caudal vein below the aorta, and in this part a fresh series of processes originates on each side from the hæmal tissue adjoining the cartilaginous sheath of the notochord, and eventually, by the junction of the processes of the two sides, a canal which contains the aorta and caudal vein is formed below the notochord. These processes for a few segments coexist with small ribs (videPl.13, fig. 10), a fact which shews (1) that they cannot be regarded as modified ribs, and (2) that the tissue from which they spring is to be viewed as a kind of general basis for all the hæmal processes which may arise, and is not specially connected with any one set of processes.
While these changes (all of which are effected during stage P) are taking place in the arches, the tissue of the vertebral bodies or cartilaginous investment of the notochord, though much thicker than before, still remains as a continuous tube whose wall exhibits no segmental differentiations.
It is in stage Q that these differentiations first appear in the vertebral regions opposite the origin of the neural arches. The outermost part of the cartilage at these points becomes hyaline and almost undistinguishable in structure from the tissue of the arches[241]. These patches of hyaline cartilage grow larger and cause the vertebral parts of the column to constrict the notochord, whilst the intervertebral parts remain more passive, but become composed of cells with very little intercellular substance. Coincidently also with these changes, part of the layer internal to the hyaline cartilage becomes modified to form a somewhat peculiar tissue, the intercellular substance of which does not stain, and in which calcification eventually arises (Pl.13, fig. 11). The innermost layer adjoining the notochord retains its primitivefibrous character, and is distinguishable as a separate layer through both the vertebral and the intervertebral regions. As a result of these changes a transverse section through the centre of the vertebral regions now exhibits three successive rings (videPl.13, fig. 11), an external ring of hyaline cartilage invested by“the membrana elastica externa”(m.el), followed by a ring of calcifying cartilage, and internal to this a ring of fibrous cartilage, which adjoins the now slightly constricted notochord. A transverse section of an intervertebral region shews only a thick outer and thin inner ring of fibrous cartilage, the latter in contact with the sheath of the unconstricted notochord.
The constriction of the notochord proceeds till in the centre of the vertebræ it merely forms a fibrous band. The tissue internal to the calcifying cartilage then becomes hyaline, so that there is formed in the centre of each vertebral body a ring of hyaline cartilage immediately surrounding the fibrous band which connects the two unconstricted segments of the notochord. The intervertebral tissue becomes more and more fibrous. In Cartier's paper before quoted there is a figure (fig. 3) which represents the appearance presented by a longitudinal section of the vertebral column at this stage.
The relation of the vertebral bodies to the arches requires a short notice. The vertebral hyaline cartilage becomes almost precisely similar to the tissue of the arches, and the result is, that were it not for the "membrana elastica externa" it would be hardly possible to distinguish the limits of the two tissues. This membrane however persists till the hyaline cartilage has become a very thick layer (Pl.13, fig. 11), but I have failed to detect it in the adult, so that I cannot there clearly distinguish the arches from the body of the vertebræ. From a comparison however of the adult with the embryo, it is clear that the arches at most form but a small part of what is usually spoken of as the body of the vertebræ.
The changes in the notochord itself during the stages subsequent to K are not of great importance. The central part retains for some time its previous structure, being formed of large vacuolated cells with an occasional triangular patch of protoplasm containing the starved nucleus and invested by indurated layers of protoplasm. These indurated layers are allfused, and are probably rightly regarded by Gegenbaur and Götte as representing a sparse intercellular matter. The external protoplasmic layer of the notochord ceases shortly after stage K to exhibit any traces of a division into separate cells, but forms a continuous layer with irregular prominences and numerous nuclei (Pl.13, fig. 9). In the stages subsequent to P further changes take place in the notochord: the remains of the cells become more scanty and the intercellular tissue assumes a radiating arrangement, giving to sections of the notochord the appearance of a number of lines radiating from the centre to the periphery (Pl.13, fig. 11).
The sheath of the notochord at first grows in thickness, and during stage L there is no difficulty in seeing in it the fine radial markings already noticed by Müller[242]and Gegenbaur[243], and regarded by them as indicating pores. Closely investing the sheath of the notochord there is to be seen a distinct membrane, which, though as a rule closely adherent to the sheath, in some examples separates itself from it. It is perhaps the membrane identified by W. Müller[244](though not by Gegenbaur) as Kölliker's“membrana elastica interna”. After the formation of the cartilaginous investment of the notochord, this membrane becomes more difficult to see than in the earlier stage, though I still fancy that I have been able to detect it. The sheath of notochord also appears to me to become thinner, and its radial striation is certainly less easy to detect[245].
EXPLANATION OF PLATE 13.
Complete List of Reference Letters.
al.Alimentary tract.ao.Aorta.c.Connective tissue.cav.Cardinal vein.ch.Notochord.ep.Epiblast.ha.Hæmal arch.l.Liver.ll.Lateral line.mc.Mucous canal of the head.mel.Membrana elastica externa.mp.Muscle-plate.mp´.Muscles of muscle-plate.na.Neural arch.nl.Nervus lateralis.rp.Rib process.sd.Segmental duct.sh.Sheath of notochord.spc.Spinal cord.spg.Spinal ganglion.syg.Sympathetic ganglion.um.Ductus choledochus.v.Blood-vessel.var.Vertebral arch.vb.Vertebral body.vcau.Caudal vein.vin.Intestinal branch of the vagus.vop.Ramus ophthalmicus of the fifth nerve.x.Subnotochordal rod.
Fig. 1. Section through the anterior part of an embryo ofScyllium caniculaduring stage L.
c.Peculiar large cells which are found at the dorsal part of the spinal cord. Sympathetic ganglion shewn atsyg. Zeiss A,ocul.1.
Fig. 2. Section through the lateral line at the time of its first formation.
The cells markednlwere not sufficiently distinct to make it quite certain that they really formed part of the lateral nerve. Zeiss B,ocul.2.
Figs. 3a, 3b, 3c, 3d. Four sections of the lateral line from an embryo belonging to stage L. 3ais the most anterior. In 3athe lateral nerve (nl) is seen to lie in the mesoblast at some little distance from the lateral line. In 3band 3cit lies in immediate contact with and partly enclosed by the modified epiblast cells of the lateral line. In 3d, the hindermost section, the lateral line is much larger than in the other sections, but no trace is present of the lateral nerve. The sections were taken from the following slides of my series of the embryo (the series commencing at the tail end) 3d(46), 3c(64), 3b(84), 3a(93). The figures all drawn on the same scale, but 3ais not from the same side of the body as the other sections.
Fig. 4. Section through lateral line of an embryo of stage P at the point where it is acquiring an opening to the exterior. The peculiar modified cells of its innermost part deserve to be noticed. Zeiss D,ocul.2.
Fig. 5. Mucous canals of the head with branches of the ramus ophthalmicus growing towards them. Stage O. Zeiss A,ocul.2.
Fig. 6. Mucous canals of head with branches of the ramus ophthalmicus growing towards them. Stage between O and P. Zeiss a a,ocul.2.
Fig. 7. Junction of a nerve and mucous canal. Stage P. Zeiss D,ocul.2.
Fig. 8. Longitudinal and horizontal section through the muscle-plates and adjoining structures at a stage intermediate between L and M. The section is intended to shew the gradual conversion of the cells of the somatic layer of muscle-plates into muscles.
Fig. 9. Longitudinal section through the notochord and adjoining parts to shew the first appearance of the cartilaginous notochordal sheath which forms the vertebral centra. Stage N.
Fig. 10. Transverse section through the tail of an embryo of stage P to shew the coexistence of the rib-process and hæmal arches in the first few sections behind the point where the latter appear. Zeiss C,ocul.1.
Fig. 11. Transverse section through the centre of a caudal vertebra of an embryo somewhat older than Q. It shews (1) the similarity between the arch-tissue and the hyaline tissue of the outer layer of the vertebral centrum, and (2) the separation of the two by the membrana elastica externa[246](mel). It shews also the differentiation of three layers in the vertebral centrum:videp.374.
[228]Jenaische Zeitschrift,Vol.VIII.
[229]Entwicklungsgeschichte d. Unke.
[230]Urogenitalsystem d. Selachier.Semper'sArbeiten, Bd.II.
[231]Loc. cit.p. 398.
[232]Götte extends his statements about the lateral nerve to the nerves supplying the mucous canals in the head; but my observations appear to me, as far as Elasmobranchii are concerned, nearly conclusive against such a derivation of the nerves in the head.
[233]I believe that Götte, amongst his very numerous valuable remarks in theEntwicklungsgeschichte der Unke, has put forward a view similar to this, though I cannot put my hand on the reference.
[234]The difference between Dr Götte's account of the development of the muscles and my own consists mainly in my attributing to the somatic layer of the muscle-plates a share in the formation of the great lateral muscles, which he denies to it. In an earlier section of this Monograph,pp.333,334, too much stress was unintentionally laid on the divergence of our views; a divergence which appears to have, in part at least, arisen, not from our observations being opposed, but from Dr Götte's having taken the highly differentiated Bombinator as his type instead of the less differentiated Elasmobranch.
[235]Das Kopfskelet d. Selachier,p.123.
[236]Entwicklungsgeschichte d. Unke,pp.433-4.
[237]Zeitschrift f. Wiss. Anat.Bd.XXV., Supplement.
[238]Videpp.356,357.
[239]None of my specimens resembles this figure, and the layer when first formed is in my embryos much thinner than represented by Gegenbaur, and the histological structure of the embryonic cartilage is very different from that of the cartilage in the figures alluded to. Götte's very valuable researches with reference to the origin of this layer in Amphibians tend to confirm the view advocated in the text.
[240]In the adult Scyllium it is well known that the posterior root pierces the intercalated cartilage and the anterior root the true neural arch. This however does not seem to be the case in the embryo at stage P.
[241]A good representation of a longitudinal section at this stage is given by Cartier (Zeitschrift f. Wiss. Zoologie, Bd.XXV., SupplementPl.IV.fig. 1), who also gives a fair description of the succeeding changes of the vertebral column.
[242]Jenaische Zeitschrift,Vol.VI.
[243]Loc. cit.
[244]Loc. cit.
[245]Gegenbaur makes the reserve statement with reference to the sheath of the notochord. For my own sections the statement in the text certainly holds good. Fortunately the point is one of no importance.
[246]The slight difference observable between these two tissues in the arrangement of their nuclei has been much exaggerated by the engraver.
The spinal nerves.
The development of the spinal nerves has been already treated by me at considerable length in a paper read before the Royal Society in December, 1875[247], and I have but little fresh matter to add to the facts narrated in that paper. The succeeding account, though fairly complete, is much less full than the previous one in thePhilosophical Transactions, but a number of morphological considerations bearing on this subject are discussed.
The rudiments of the posterior roots make their appearance considerably before those of the anterior roots. They arise during stage I, as outgrowths from the spinal cord, at a time when the muscle-plates do not extend beyond a third of the way up the sides of the spinal cord, and in a part where no scattered mesoblast-cells are present. They are formed first in the anterior part of the body and successively in the posterior parts, in the following way. At a point where a spinal nerve is about to arise, the cells of the dorsal part of the cord begin to proliferate, and the uniform outline of the cord becomes broken (Pl.14, fig. 3). There is formed in this way a small prominence of cells springing from the summit of the spinal cord, and constituting a rudiment of a pair of posterior roots. In sections anterior to the point where a nerve is about to appear, the nerve-rudiments are always very distinctly formed. Such a section is shewn inPl.14, fig. 2, and the rudiments may there be seenas two club-shaped masses of cells, which have grown outwards and downwards from the extreme dorsal summit of the neural canal and in contact with its walls. The rudiments of the two sides meet at their point of origin at the dorsal median line, and are dorsally perfectly continuous with the walls of the canal.
It is a remarkable fact that rudiments of posterior roots are to be seen in every section. This may be interpreted as meaning that the rudiments are in very close contact with each other, but more probably means, as I hope to shew in the sequel, that there arises from the spinal cord a continuous outgrowth from which discontinuous processes (the rudiments of posterior roots) grow out.
After their first formation these rudiments grow rapidly ventralwards in close contact with the spinal cord (videPl.14, fig. 1, andPl.11, figs. 6 and 7), but soon meet with and become partially enclosed in the mesoblastic tissue (Pl.11, fig. 7). The similarity of the mesoblast and nerve-tissue in Scyllium and Pristiurus embryos hardened in picric or chromic acid, render the nerves in these genera, at the stage when they first become enveloped in mesoblast, difficult objects to observe; but no similar difficulty is encountered in the case of Torpedo embryos.
While the rudiments of the posterior roots are still quite short, those of the anterior roots make their first appearance. Each of these (Pl.14, fig. 4,a.r.) arises as a very small but distinct conical outgrowth from a ventral corner of the spinal cord. From the very first the rudiments of the anterior roots have an indistinct form of peripheral termination and somewhat fibrous appearance, while the protoplasm of which they are composed becomes attenuated towards its end. The points of origin of the anterior roots from the spinal cord are separated by considerable intervals. In this fact, and also in the fact of the nerves of the two sides never being united with each other in the median line, the anterior roots exhibit a marked contrast to the posterior. There are thus constituted, before the close of stage I, the rudiments of both the anterior and posterior roots of the spinal nerves. The rudiments of both of these take their origin from the involuted epiblast of the neural canal, and the two roots of each spinal nerve are at first quite unconnectedwith each other. It is scarcely necessary to state that the pairs of roots correspond in number with the muscle-plates.
It is not my intention to enter with any detail into the subsequent changes of the rudiments whose origin has been described, but a few points especially connected with their early development are sufficiently important to call for attention.
One feature of the posterior roots at their first formation is the fact that they appear as processes of a continuous outgrowth of the spinal cord. This state of affairs is not of long continuance, and before the close of stage I each posterior root has a separate junction with the spinal cord. What then becomes of the originally continuous outgrowth? It has not been possible for me to trace the fate of this step by step; but the discovery that at a slightly later period (stage K) there is present a continuous commissure independent of the spinal cord connecting the dorsal and central extremities of all the spinal nerves, renders it very probable that the original continuous outgrowth becomes converted into this commissure. Like all the other nervous structures, this commissure is far more easily seen in embryos hardened in a mixture of osmic and chromic acids or osmic acid, than in those hardened in picric acid. Its existence must be regarded as one of the most remarkable results of my researches upon the Elasmobranch nervous system. At stage K it is fairly thick, though it becomes much thinner at a slightly later period. Its condition during stage K is shewn inPl.12, fig. 18,com. What it has been possible for me to make out of its eventual fate is mentioned subsequently[248].
A second feature of the earliest condition of the posterior roots is their attachment to the extreme dorsal summit of the spinal cord—a point of attachment very different from that which they eventually acquire. Before the commencement of stage K this state of things has become altered; and the posterior roots spring from the spinal cord in the position normal for Vertebrates.
This apparent migration caused me at first great perplexity,and I do not feel quite satisfied that I have yet got completely to the bottom of its meaning. The explanation which appears to me most probable has suggested itself in the course of some observations on the development of the thin roof of the fourth ventricle. A growth of cells appears to take place in the median dorsal line of the roof of the spinal cord. This growth tends to divaricate the two lateral parts of the cord, which are originally contiguous in the dorsal line, and causes therefore the posterior roots, which at first spring from the dorsal summit, to assume an apparent attachment to the side of the cord at some little distance from the summit. If this is the true explanation of the change of position which takes place, it must be regarded as due rather to peculiar growths in the spinal cord, than to any alteration in the absolute attachment of the nerves.
By stage K the rudiment of the posterior root has become greatly elongated, and exhibits a division into three distinct portions (Pl.14, fig. 6):
(1) A proximal portion, in which is situated the pedicle of attachment to the wall of the neural canal.
(2) An enlarged portion, which may conveniently from its future fate be called the spinal ganglion.
(3) A distal portion beyond this.
The proximal portion presents a fairly uniform diameter, and ends dorsally in a rounded expansion; it is attached, remarkably enough,not by its extremity, but by its side, to the spinal cord. The dorsal extremities of the posterior roots are therefore free.It seems almost certain that the free dorsal extremities of these roots serve as the starting points for the dorsal commissure before mentioned, which connects the roots together. The attachment of the posterior nerve-root to the spinal cord is, on account of its small size, very difficult to observe. In favourable specimens there may however be seen a distinct cellular prominence from the spinal cord, which becomes continuous with a small prominence on the lateral border of the nerve-root near its distal extremity. The proximal extremity of the rudiment is composed of cells, which, by their small size and circular form, are easily distinguished from those which form the succeeding or ganglionic portion of the nerve. This succeeding part has a swollen configuration, and is composedof large elongated cells with oval nuclei. The remainder of the rudiment forms the commencement of the true nerve.
The anterior root, which, at the close of stage I, formed a small and inconspicuous prominence from the spinal cord, grows rapidly during the succeeding stages, and soon forms an elongated cellular structure with a wide attachment to the spinal cord (Pl.14, fig. 5). At first it passes obliquely and nearly horizontally outwards, but, before reaching the muscle-plate of its side, takes a bend downwards (Pl.14, fig. 7).
I have not definitely made out when the anterior and posterior roots unite, but this may easily be seen to take place before the close of stage K (Pl.12, fig. 18).
One feature of some interest with reference to the anterior roots, is the fact that they arise not vertically below, but alternately with the dorsal roots, a condition which persists in the adult.
Although I have made some efforts to determine the eventual fate of the commissure uniting the dorsal roots, these have not hitherto been crowned with success. It grows thinner and thinner, becoming at the same time composed of fibrous protoplasm with imbedded nuclei (Pl.14, figs. 8 and 9). By stage M it is so small as to be quite indistinguishable in transverse sections; and I have failed in stage P to recognize it at all. I can only conclude that it gradually atrophies, and finally vanishes without leaving a trace. Both its appearance and history are very remarkable, and deserve the careful attention of future investigators.
There can be little doubt that it is some sort of remnant of an ancestral structure in the nervous system; and it would appear to indicate that the central nervous system must originally have been formed of a median and two lateral strands. At the same time I very much doubt whether it can be brought into relation with the three rows of ganglion-cells (a median and two lateral) which are so frequently present on the ventral side of annelidan nerve-cords.
My results may be summarised as follows:—Along the extreme dorsal summit of the spinal cord there arises on each side a continuous outgrowth. From each outgrowth processes corresponding in number to the muscle-plates grow downwards.These are the rudiments of the posterior nerve-roots. The outgrowths, though at first attached to the spinal cord throughout their whole length, soon cease to be so, and remain in connection with it at certain points only, which form the primitive junctions of the posterior roots with the spinal cord. The original outgrowth on each side remains as a bridge, uniting together the dorsal extremities of all the posterior roots. The posterior roots, though primitively attached to the dorsal summit of the spinal cord, eventually come to arise from its sides. The original homogeneous rudiments before the close of stage K become differentiated into a root, a ganglion, and a nerve.
The anterior roots, like the posterior, are outgrowths from the spinal cord, but are united independently with it, and the points from which they spring originally, remain as those by which they are permanently attached. The anterior roots arise, not vertically below, but in the intervals between the posterior roots. They are at first quite separate from the posterior roots; but before the close of stage K a junction is effected between each posterior root and the corresponding anterior root. The anterior root joins the posterior at some little distance below its ganglion.
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The results here arrived at are nearly in direct opposition to those of the majority of investigators, though in accordance, at least so far as the posterior roots are concerned, with the beautiful observations of Hensen 'on the Development of Mammalia[249].'
Mr Marshall[250]has more recently published a paper on the development of the nerves in Birds, in which he shews in a most striking manner that the observations recorded here for Elasmobranchii hold good for the posterior roots of Birds. The similarity between his figures and my own is very noticeable. A further discussion of the literature would be quite unprofitable, and I proceed at once to certain considerations suggested by the above observations.
General considerations.One point of general anatomy upon which my observations throw considerable light, is theprimitive origin of nerves. So long as it was admitted that the spinal and cerebral nerves developed in the embryo independently of the central nervous system, their mode of origin always presented to my mind considerable difficulties. It never appeared clear how it was possible for a state of things to have arisen in which the central nervous system as well as the peripheral terminations of nerves, whether motor or sensory, were formed independently of each other; while between them a third structure was developed, which, growing out either towards the centre or towards the periphery, ultimately brought the two into connection. That such a condition could be a primitive one seemed scarcely possible.
Still more remarkable did it appear, on the supposition that the primitive mode of formation of these parts was represented in the developmental history of Vertebrates, that we should find similar structural elements in the central and in the peripheral nervous systems. The central nervous system arises from the epiblast, and yet contains precisely similar nerve-cells and nerve-fibres to the peripheral nervous system, which, when derived from the mesoblast, was necessarily supposed to have an origin completely different from that of the central nervous system. Both of these difficulties are to a great extent removed by the facts of the development of these parts in Elasmobranchii.
It is possible to suppose that in their primitive differentiation contractile and sensory systems may, as in Hydra[251], have been developed from the protoplasm of even the same cell. As the sensory and motor systems became more complicated, the sensory portion of a cell would become separated by an increasing interval from the muscular part of a cell, and the two parts of a cell would only be connected by a long protoplasmic process. When such a condition as that was reached, the sensory portion of the cell would be called a ganglion-cell or terminal sensory organ, the connecting process a nerve, and the contractile portion of the cell a muscle-cell. When these organs were in this condition, it might not impossibly happen for the general developmental growth which tended to separate theganglion-cell and the muscle-cell to be so rapid as to render it impossible for the growth of the connecting nerve to keep pace with it, and that thus the process connecting the ganglion-cell and the muscle-cell might become ruptured. Nevertheless the tendency of the process to grow from the ganglion-cell to the muscle-cell, would remain, and when the rapid developmental growth had ceased, the two would become united again by the growth of the process which had previously been ruptured. It will be seen that this hypothesis, which I have considered only with reference to a single nerve and muscle-cell, might be extended so as to apply to a complicated central nervous system and peripheral nerves and muscles, and also could apply equally as well to the sensory as to the motor terminations of a nerve. In the case of the sensory termination, we should only have to suppose that the centre nervous cell became more and more separated by the general growth from the recipient terminal sensory cell, and that during the general growth the connection between the two was mechanically ruptured but restored again on the termination of the more rapid growth.
As the descendants of the animal in which the rupture occurred became progressively more complicated, the two terminal cells must have become widely separated at a continually earlier period, till finally they may have been separated at a period of development when they were indistinguishable from the surrounding embryonic cells; and since the rupture would also occur at this period, the primitive junction between the nerve-centre and termination would escape detection. The object of this hypothesis is to explain the facts, so far as they are known, of the development of the nervous system in Vertebrates.
In Vertebrates we certainly appear to have an outgrowth from the nervous system, which eventually becomes united with the muscle or sensory terminal organs. The ingenious hypothetical scheme of development of the nerves given by Hensen[252]would be far preferable to the one suggested if it could be brought into conformity with the facts. There is, however, at present no evidence for Hensen's view, as he himself admits, but considering how little we know of the finer details of the development of nerves, it seems not impossible that suchevidence may be eventually forthcoming. The evidence from my own observation is, so far as it goes, against it. At a time anterior to the outgrowth of the spinal nerves, I have shewn[253]that the spinal cord is completely invested by a delicate hyaline membrane. It is difficult to believe that this is pierced by a number of fine processes, which completely escape detection, but which must, nevertheless, be present on the hypothesis of Hensen.
The facts of the development of nerves in Vertebrates are unquestionably still involved in considerable doubt. It may, I think, be considered as certain, that in Elasmobranchii the roots of the spinal and cranial nerves are outgrowths of the central nervous system. How the final terminations of the nerves are formed is, however, far from being settled. Götte[254], whose account of the development of the spinal ganglia is completely in accordance with the ordinary views, yet states[255]that the growth of the nerve fibres themselves is a centrifugal one from the ganglia. My own investigations prove that the ganglia have a centrifugal development, and also appear to demonstrate that the nerves themselves near the ganglion have a similar manner of growth. Moreover, the account given in the preceding chapter of the manner in which the nerves become connected with the mucous canals of the head, goes far to prove that the whole growth of the nerves is a centrifugal one. The combination of all these converging observations tells strongly in favour of this view.
On the other hand, Calberla[256]believes that in the tails of larval Amphibians he has seen connective-tissue cells unite with nerve-processes, and become converted into nerves, but he admits that he cannot definitely prove that the axis-cylinder has not a centrifugal growth, while the connective-tissue cells merely become converted into the sheath of the nerve. If Calberla's view be adopted, that the nerves are developed directly out of a chain of originally indifferent cells, each cell of the chain being converted in turn into a section of the nerve, an altogether different origin of nerves from that I have just suggested would seem to be indicated.
The obvious difficulty, already alluded to, of understanding how it is, according to the generally accepted mode of development of the spinal nerves, that precisely similar nerve-cells and nerves should arise in structures which have such different origins as the central nervous system and the spinal nerves, is completely removed if my statements on the development of the nerves in Elasmobranch represent the truth.
One point brought out in my investigations appears to me to have bearings upon the origin of the central canal of the vertebrate nervous system, and in consequence upon the origin of the vertebrate nervous system itself. This point is, that the posterior nerve-rudiments make their first appearance at the extreme dorsal summit of the spinal cord. The transverse section of the ventral nervous cord of an ordinary segmented Annelid consists of two symmetrical halves placed side by side. If by a mechanical folding the two lateral halves of the nervous cord became bent towards each other, while into the groove between the two the external skin became pushed, we should have an approximation to the vertebrate nervous system. Such a folding as this might take place to give extra rigidity to the body in the absence of a vertebral column.
If this folding were then completed in such a way that the groove, lined by external skin and situated between the two lateral columns of the nervous system, became converted into a canal, above and below which the two columns of the nervous system united, we should have in the transformed nervous cord an organ strongly resembling the spinal cord of Vertebrates.
It is well known that the nerve-cells are always situated on the ventral side of the abdominal nerve-cord of Annelids, either as a continuous layer, or in the form of two, or more usually, three bands. The dorsal side of the cord is composed of nerve-fibres or white matter. If the folding I have supposed were to take place in the Annelid nervous cord, the grey and white matters would have very nearly the same relative situations as they have in the Vertebrate spinal cord. The grey matter would be situated in the interior and line the central canal, and the white matter would nearly surround the grey. The nerves would then arise, not from the sides of the nervous cord as in existing Annelids, but from its extreme ventral summit. Oneof the most striking features which I have brought to light with reference to the development of the posterior roots, is the fact of their growing out from the extreme dorsal summit of the neural canal, a position analogous to the ventral summit of the Annelidan nervous cord. Thus the posterior roots of the nerves in Elasmobranchii[257]arise, in the exact manner which might have been anticipated, were the spinal canal due to such a folding as I have suggested.
The argument from the position of the outgrowth of nerves becomes the more striking from its great peculiarity, and forms a feature which would be most perplexing without some such explanation as I have proposed. The central epithelium of the neural canal, according to this view, represents the external skin, and its ciliation in certain cases may, perhaps, be explained as a remnant of the ciliation of the external skin still found amongst many of the lower Annelids.
I have employed the comparison of the Vertebrate and Annelidan nervous cords, not so much to prove a genetic relation between the two, as to shew theà prioripossibility of the formation of a spinal cord, and theà posteriorievidence we have of the vertebrate canal having been formed in the way indicated. I have not made use of what is really my strongest argument,viz.that the embryological mode of formation of the spinal canal by a folding in of the external epiblast is the very method by which I supposed the spinal canal to have been formed in the ancestors of Vertebrates. My object has been to suggest a meaning for the peculiar primitive position of the posterior roots, rather than to attempt to explain in full the origin of the spinal canal.
Although the homologies between the Vertebrate and the Annelidan nervous systems are not necessarily involved in the questions which arise with reference to the formation of the spinal canal, they have nevertheless considerable bearings on it.
Two views have recently been put forward on this subject.Professor Gegenbaur[258]looks upon the central nervous system of Vertebrates as equivalent to the superior œsophageal ganglia of Annelids and Arthropods only, while Professors Leydig[259]and Semper[260]and Dr Dohrn[261]compare it with the whole Annelidan nervous system.
The first of these two views is only possible on the supposition that Vertebrates are descended from unsegmented ancestors, and even then presents considerable difficulties. If the ancestors of Vertebrates were segmented animals, and several of the recent researches tend to shew that they were, they must almost certainly have possessed a nervous cord like that of existing Annelids. If such were the case, it is almost inconceivable that the greater portion of the nervous system which forms the ventral cord can have become lost, and the system reduced to the superior œsophageal ganglia. Dr Dohrn[262], who has speculated very profoundly on this matter, has attempted to explain and remove some of the difficulties which arise in comparing the nervous systems of Vertebrates and Annelids. He supposes that the segmented Annelids, from which Vertebrates are descended, were swimming animals. He further supposes that their alimentary canal was pierced by a number of gill-slits, and that the anterior amongst these served for the introduction of nutriment into the alimentary canal, in fact as supplementary mouths as well as for respiration. Eventually the old mouth and throat atrophied, and one pair of coalesced gill-slits came to serve as the sole mouth. Thus it came about that on the disappearance of that portion of the alimentary canal, which penetrated the œsophageal nervous ring, the latter structure ceased to be visible as such, and no part of the alimentarycanal was any longer enclosed by a commissure of the central nervous system. With the change of mouth Dr Dohrn also supposes that there took place a change, which would for a swimming animal be one of no great difficulty, of the ventral for the dorsal surface. This general explanation of Dr Dohrn's, apart from the considerable difficulty of the fresh mouth, appears to me to be fairly satisfactory. Dr Dohrn has not however in my opinion satisfactorily dealt with the questions of detail which arise in connection with this comparison. One of the most important points for his theory is to settle the position where the nervous system was formerly pierced by the œsophagus. This position he fixes in the fourth ventricle, and supports his hypothesis by the thinness of the roof of the spinal canal in this place, and the absence (?) of nervous structures in it.
It appears to me that this thinness cannot be used as an argument. In the first place, if the hypothesis I have suggested as to the formation of the spinal canal be accepted, the formation of the canal must be supposed to have occurred in point of time either after or before the loss of the primitive mouth. If, on the one hand, the spinal canal made its appearance before the atrophy of the primitive mouth, the folding to form it must necessarily have ceased behind the mouth; and, on the supposition of the œsophageal ring having been situated in the region of the fourth ventricle, a continuation of the spinal canal could not be present in front of this part. If, on the other hand, the cerebro-spinal canal appeared after the disappearance of the primitive mouth, its roof must necessarily also be a formation subsequent to the atrophy of the mouth, and varieties of structure in it can have no bearing upon the previous position of the mouth.
But apart from speculations upon the origin of the spinal cord, there are strong arguments against Dr Dohrn's view about the fourth ventricle. In the first place, were the fourth ventricle to be the part of the nervous system which previously formed the œsophageal commissures, we should expect to find the opening in the nervous system at this point to be visible at an early period of development, and at a later period to cease to be so. The reverse is however the case. In early embryonic life the roof of the fourth ventricle is indistinguishable from otherparts of the nervous system, and only thins out at a later period. Further than this, any explanation of the thin roof of the fourth ventricle ought also to elucidate the nearly similar structure in the sinus rhomboidalis, and cannot be considered satisfactory unless it does so.
The peculiarities of the cerebro-spinal canal in the region of the brain appear to me to present considerable difficulties in the way of comparing the central nervous system of Vertebrates and segmented Annelids. The manner in which the cerebro-spinal canal is prolonged into the optic vesicles, the cerebral and the optic lobes is certainly opposed both to an intelligible explanation of the spinal canal itself, and also to a comparison of the two nervous systems under consideration.
Its continuation into the cerebral hemispheres and into the optic lobes (mid-brain) may perhaps be looked upon as due to peculiar secondary growths of those two ganglia, but it is very difficult to understand its continuation into the optic vesicles.
If it be granted that the spinal canal has arisen from a folding in of the external skin, then the present inner surface of the optic vesicle must also have been its original outer surface, and it follows as a necessary consequence that the present position of the rods and cones behind and not in front of the nervous structures of the retina was not the primitive one. The rods and cones arise, as is well known, from the inner surface of the outer portion of the optic vesicle, and must, according to the above view, be supposed originally to have been situated on the external surface, and have only come to occupy their present position during the folding in, which resulted in the spinal canal. Onà priorigrounds we should certainly expect the rods and cones to have resulted from the differentiation of a layer of cells external to the conducting nervous structures. The position of the rods and cones posterior to these suggests therefore that some peculiar infolding has occurred, and may be used as an argument to prove that the medullary groove is no mere embryonic structure, but the embryonic repetition of an ancestral change. The supposition of such a change of position in the rods and cones necessarily implies that the folding in to form the spinal canal must have been a very slow one. It must have given time to the refracting media of the eyegradually to travel round, so as still to maintain their primitive position, while in successive generations a rudimentary spinal furrow carrying with it the retina became gradually converted into a canal[263].
If Dr Dohrn's comparison of the vertebrate nervous system with that of segmented Annelids be accepted, the following two points must in my opinion be admitted:—
(1) That the formation of the cerebro-spinal canal was subsequent to the loss of the old mouth.
(2) That the position of the old mouth is still unknown.
The well-known view of looking at the pituitary and pineal growths as the remnants of the primitive œsophagus, has no doubt some features to recommend it. Nearly conclusive against it is the fact that the pituitary involution is not, as used to be supposed, a growth towards the infundibulum of the hypoblast of the œsophagus, but of the epiblast of the mouth. It is almost inconceivable that an involution from the present mouth can have assisted in forming part of the old œsophagus.
There is a view not involving the difficulty of the œsophageal ring, fresh mouth[264], and of the change of the ventral to the dorsalsurface, which, though so far unsupported by any firm basis of observed facts, nevertheless appears to me worth suggesting. It assumes that Vertebrates are descendednotthrough the present line of segmented Vermes, but through some other line which has now, so far as is known, completely vanished. This line must be supposed to have originated from the sameunsegmented Vermesas the present segmented Annelids. They therefore acquired fundamentally similar segmental and other Annelidan organs.
The difference between the two branches of the Vermes lay in the nervous system. The unsegmented ancestors of thepresentAnnelids seem to have had a pair of super-œsophageal ganglia, from which two main nervous stems extended backwards, one on each side of the body. Such a nervous system in fact as is possessed by existing Nemertines or Turbellarians[265]. As the Vermes became segmented and formed the Annelids, these side nerves seem to have developed ganglia, corresponding in number with the segments, and finally, approximating on the ventral surface, to have formed the ventral cord[266].
The other branch of Vermes which I suppose to have been the ancestors of Vertebrates started from the same stock as existing Annelids, but I conceive the lateral nerve-cords, instead of approximating ventrally, to have done so dorsally, and thus a dorsal cord to have become formed analogous to the ventral cord of living Annelids, only without an œsophageal nerve-ring[267].
It appears to me, (if the difficulties of comparing the Annelidan ventral cord with the spinal cord of Vertebrates are found to be insurmountable), that this hypothesis would involve far fewer improbabilities than one which supposes the whole central nervous system of Vertebrates to be homologous with the super-œsophageal ganglia. The mode of formation of a nervous system presupposed in my hypothesis, well accords with what we know of the formation of the ventral cord in existing Annelids.
The supposition of the existence of another branch of segmented Vermes is not a very great difficulty. Even at the present day we have possibly more than one branch of Vermes which have independently acquired segmentation.viz.: the Chætopodous Annelids and the Hirudinea. If the latter is an isolated branch, it is especially interesting from having independently developed a series of segmental organs like those of Chætopodous Annelids, which we must suppose the ancestors of Vertebrates also to have done if they too form an independent branch.
In addition to the difficulty of imagining a fresh line of segmented Vermes, there is another difficulty to my view,viz.: the fact that in almost all Vermes, the blood flows forwards in the dorsal vessel, and backwards in the ventral vessel. This condition of the circulation very well suits the view of a change of the dorsal for the ventral surfaces, but is opposed to these surfaces being the same for Vertebrates and Vermes. I cannot however regard this point as a very serious difficulty to my view, considering how undefined is the circulation in the unsegmented groups of the Vermes.