Paper - Vertebrate cephalogenesis 1 (1890)

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Ayers H. Concerning vertebrate cephalogenesis. (1890) J Morphol. 4: 221-245.

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This 1890 historic paper by Ayers describes hearing and head development in several species including human. Note that this review contains extensive untranslated quotes from the earlier German literature.



Also by this author: Ayers H. Vertebrate cephalogenesis, II. A contribution to the morphology of the vertebrate ear, with a reconsideration of its functions . (1892) J Morphol. 6(3): 1-360.

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Concerning Vertebrate Cephalogenesis

Howard Ayers.


In this short resume of some of the results of my investigations in vertebrate cephalogenesis, I shall not give a complete account of the morphological data upon which the conclusions are based ; but shall introduce only such facts as seem necessary for this presentation.


A more detailed account with a critical consideration of the literature bearing upon the subject is reserved for a more extended and illustrated publication which I have in preparation.


The problem of the origin of the vertebrate head, more especially the brain, from the invertebrate type is, so far as our knowledge yet reaches, an insoluble one ; but given the vertebrate type of body and central nervous system, we are in position to clearly demonstrate its phylogenetic outcome as represented in the mammalian head and brain.


Starting with the central nervous system of Amphioxus, we have to deal with an organ which affords many points of contrast with the axial nervous system of higher vertebrates and which serves, as some authorities think, to bridge over the chasm between the invertebrate type (arthropod and annelid) and the vertebrate.


With the exception of an undetermined small number of anterior segments, the nerve cord of Amphioxus is divided up into a series of physiologically equal segments as Steiner has shown ; but I feci confident from anatomical facts that further and more detailed experimentation will show that there are some modifications to be introduced into Steiner's results, and that there are differentiations physiologically which the crude methods of experiment used by him excluded from the physiological reaction. Steiner's results on other vertebrates would lead to a conclusion differing from that which he has published with ref^ard to Amphioxus. For in bis experiments on Amphioxus he was unable to take into account any of the higher seose organs. Of course their relation to locomotion and the central mechanism effecting this relation entirely escaped him.


I hope to show that there are certain ganghonic centres in the anterior end of the nerve cord of Amphioxus, which compel us to call this region a brain strictly comparable with that of other vertebrates; for in this region we have the centres of special sense brought into relation with locomotion.


!n my final paper I shall give an historical review of the ideas that have been held concerning vertebrate cephalogenesis. For it is in the gradual evolution of these ideas that we have the firmest support, and completest precedent, for leaving the prevailing ideas for those that can be shown to come nearer the truth in nature. The idea that the human skull (as typical of the highest vertebrates and hence erroneously thought to most certainly present genuine vertebrate conditions) was formed of relatively slightly modified vertebral bodies and their processess, had its eminent exponents and ran its course. It was succeeded by the theory that it was only in the cartilaginous cranium that remnants of primitive segments were to be sought. This form of solution was modified by the statement that only a portion of the primordial cranium could possibly show traces of the primitive segmented character.


This brings me to the expression of the view, which has firm support in facts, that the primordial cranium is never influenced by vertebral segmentation, as it appears in, and belongs to, a stage antecedent to the formation of vertebrw ; further, that it is not primarily influenced by the mesomeric segmentation of the body, since it arose at a later period phylogenetically and after the mesomery ontogenetically. The primordial cranium has been gradually acquired by vertebrates, and its rudiments were developed first in or near the horizontal plane in which the chorda lies, E.ttending in a direction more or less parallel to the chorda, it does not necessarily show traces of the primitive segmentation of that part of the body in which it is developed, since many, at least, of the features of segmentation, had long vanished before a protecting cranium formed about the nervous axis. In such a structure wc would expect coenogenetic (ontogenetic) variations to be of frequent occurrence.


What I have said above does not exclude the possibility of the inclusion of vertebral remains within the skull, nor is this view influenced by the fact that such inclusions are known to exist, e,g, in the cartilaginous fishes, etc., and for this reason ; the skull is formed about the brain and includes various organs, not always the same, within its substance. As illustrations of the variations met with, we have in some cases the aorta included in the cartilaginous basis cranii, though usually it is left out, the notochord usually for the whole of its cranial length, though it may be left out in part, as for example its anterior end may lie below the cartilage or above, ue, inside the cranial cavity either projecting beyond the pituitary prominence or running out on the inner face of the skull behind it. There are other facts of this class which have not received enough attention.

A. The anterior end of the neural axis of Amphioxus is a brain^ and corresponds with a certain definite portion of tfie brains of other vertebrates. Its anterior wall is the homologue of the lamina temtinalis of other vertebrate brains, and t/ie anterior portion of its unpaired ventricle is the thalamocosle. There is a posterior portion of the ventricle intimately associated with ^ gangliofiic tract, which corresponds to the mesoccele, while the myelocoele remains, more or less widened, varying much in different individuals, but always in an undifferentiated condition.

Although the nervous system of Amphioxus has been oftentimes studied, many features of importance remain to be described, and the well-established relations deserve reconsideration in connection with the new ones. With the improvements in . methods of preparation, results unobtainable otherwise are reached, which show that we may still hope for more light on important questions from even well-worked fields. The preparations I have studied were made by the celloidin method of imbedding and nitric acid maceration process, and I can recommend both as giving excellent results.

I may say, to begin with, that I do not consider Amphioxus to be a degraded form, in the usual sense of that word as employed in vertebrate phylogeny. Its larval modifications cannot be called degradations of structure, nor are its adult peculiarities to be looked upon in the light of degraded or bizarre modifications of normal vertebrate conditions ; on the contrary, they are to be regarded as not only normal, but also as primitive, and in a certain degree ancestral, conditions of structure.

The derivation of the vertebrate phylum from some simple type closely approaching Amphioxus, in detail of structure, in almost' all its organs, as we know them at the present time, becomes a morphological necessity. Instead of precluding the possibility of establishing the claims of Amphioxus to such position in the phylum, every advance in our knowledge of the life-history of Amphioxus serves only to strengthen such claims.

It is to be regretted that certain zoologists should have so dulled their morphological sense as to be found denying to Amphioxus any position whatsoever among vertebrates. As an offset to such rash opinions, I will only quote the words of Professor Huxley, giving his conclusions after a careful study of the anatomy of Amphioxus, and a detailed comparison with other fish forms : " In all other respects, however, it conforms (except in the absence of auditory organs) to the vertebrate type ; and considering its resemblance to the early stages of Petromyzon, ... I can see no reason for removing it from the class of Pisces." I might quote other eminent authority in favor of the strictly vertebrate nature of Amphioxus, but I think this should suffice. Surely we may never hope to know more of the mystery of the origin of vertebrates by ignoring the most important of the still accessible forms that lead us back (o the beginning of our type.

It has become necessary, in any discussion of the homologies of the vertebrate brain, to define more accurately what is to be understood by the term "vertebrate brain." Evidently the definition of the word must include the names and relations, as far as lies within the province of a definition, of all those parts common to all vertebrate forms, excluding from the principal sentence of the definition all exceptions however important. We have not lacked for definitions more or less specific, but until quite recently I do not know of any investigator who has attempted to define the organ in terms harmonious with the present condition of morphology and physiology. Steiner has shown, by a beautiful series of experiments on numerous forms, that we may only speak of a brain from the physiologist's standpoint when we have associated with the general centre of locomotion one or more of the organs of the higher senses, and this definition is entirely admissible from a morphological standpoint. While Steiner's experiments do not show the presence of a brain in Amphioxus, they do not, I think, in any way demonstrate or even render probable its absence^ and it can be shown that the morphological or physical basis required by Steiner's definition is present.


  • July 27. I have )usl teen Boreri'i paper, "Ubn die Niere des Amphioxus" . aod lince this invi:sligiiUiC bos shown in most conclusive mkonet by his iniporUnt diKOvery, that Uic kidneys of Amphioxus are anceslral structures, I am readf tu withdraw the limiting word "almoit," since it WM nuint)' with rcfciencc ti< Ihc Uidney iystem thai the rnervntion wm made.



I would define the vertebrate brain as follows : The ** vertebrate brain " is tfiat portion of the anterior part of the axial nerve cord^ associated with organs of special sense ^ containing an enlargement of the central canal which is carried out into all stnutures formed by the outgrowth of the brain wall. Its walls contain the principal centres for the co-ordination of sensations and movements. All further additions to this simple brain {Amphioxus) are made in response to the demands of the organs of special sefise^ with which is associated extension of the co-ordination apparatus. With such additions we have the compound brain of all other known vertebrates up to man inclusive.

Reasons why the anterior end of the nerve cord of Amphioxus is a brain. It is a brain because

1. It forms the anterior termination of the neural axis.

2. It stands in intimate relation to the sense organs eye and nose.

3. It gives oflf at least two pairs of sensory nerves provided with peripheral ganglia.

4. It possesses large groups of ganglion cells forming centres of co-ordination.

5. It possesses an enlarged section of the central canal in the form of an unpaired ventricle with three well marked diverticula, two optic, one olfactory.

6. It is the largest part of the nervous system, at a time when the massive musculature and branchial apparatus of the anterior middle fourth of the body has not reached the stage requiring much enlarged central accomniodations.^

1 When, however, the innervation of the locomotive apparatus (which in the a^Iult animal more than equals the remaining organs in bulk) is fully developed, the


7. It shows in young larvEE growth to such an extent as to cause a ventral flexure of the chorda, the brain itself bending downwards, thus producing a "cranial flexure,"

8. It shows in all other details of structure that it is not simply the anterior end of the spinal chord, but a brain.

g. It shows in a larval stage soon after the differentiation of fibres in the neural axis (larvas with one gill slit), a marked differentiation into ganglionic and fibrous regions, and the boundaries of the unpaired ventricle as well as the lamina terminals are distinctly marked out. There is then a ventricular segment of the brain reserved for the special sense organs. The fibres appear simultaneously with the formation of the pigment spot, and are in all probability the ways by means of which the sensations from this special sense organ are conveyed backwards to the motor centres.

10. Since Amfhioxus is a vertebrate, these relations must }iavt direct and important bearings on tkf phytogeny of the veriebratt brain and head, and will afford us invaluable aid in clearing up these intricate problems.

B, The large collections of ganglion cells just posterior to the tkalamoccele are homologous tvith the medullary nuclei of other vertebrates, since their connections show them to be centres for the control of the branchial apparatus, and the sensory and motor structures lying in the territory of the gill basket, — e.g. centrts of respiration, deglutition, etc.

These groups of large ganglion cells do not reach quite to the thalamocoele. A portion of the wall bounding the ventricle posteriorly is free from them, and is made up of such cells as are strictly comparable with the cellular elements of the midbrain of higher forms. From this narrow territory and the central canal contained in it is derived the mesencephalon and

brain ii rclatiTCly tmaUer, bul il itill lias iti peculiai ilnicture. We have othet in(Udcci of the «ctual ptepoodMance in. liie ol ciccumscribed tracti of Uie nervou axis aver the brain. In thoK ancient furms, t.g. Stegosaunu, whoie remaini have been described by Marsh and othen, wbeie the lacral canal ii ihown to Kreatljt exceed the cranial cavity in ill cubic dimeniiDU. But here there ii a doubt as to whether the nervous axis in the sacral canal really hUed the space, or whether it bore proportionately the satne relatiom to its cavity tliat the brain did \a il* cranial (pace. There is reason to senoosly doubt that the sacral enlargement of the cord was actually larger and more important than tlic ticaiTi in rclatiDU to the locomotive mechanism of mesocoele of higher forms. The cerebellum is simply a dorsal commissure of the medullary region, as has been shown by Osborne and others from studies on higher vertebrates. I have found no trace of a cerebellar commissure in Amphioxus. The open ventricle of the medulla is produced by the great increase of ganglion cells, and especially of the fibre tracts which must of necessity pass through this region in order to reach the centres of coordination in the parts anterior to it. The basal and lateral portions of its walls are thus greatly thickened, the ganglion cells of the nerve nuclei arrange themselves in harmony with these changed conditions, and the dorsal wall is greatly extended without at the same time being structurally complicated. The medulla of higher vertebrates is not co-extensive in all forms and includes a varying number of the segments represented in Amphioxus by simple spinal segments.

The brain of Amphioxus possesses all those functions which in higher vertebrates are possessed by thalamencephalon midbrain, and medulla, except an undetermined number of the posterior segments of the medulla of the higher forms. Of course these functions are all of a milder nature than in the higher animals.

The reason for Steiner's failure to find a medullary centre of co-ordination lies in the intense nature of the stimuli applied to the nervous apparatus (resection, etc.) and to the small size of the region to which the stimuli must be applied. The nervous apparatus is of such a delicate nature that such strong stimuli serve to call forth the activities of each segmental centre of locomotion, and prevent the observation of any other results of stimulation.

Much more delicate methods must be used to obtain reaction of the organs of special sense. Of the possible means of experimentation, which appear to me likely to give good results in the case of the pigment spot and the olfactive pit, are circumscribed application of bundles of light rays of varying intensity and wave lengths, and the application of olfactive stimuli by means of fine capillary tubes to the resting animals in sea-water.

C. The ontogenetic changes of the neural axis in other vertebrates carries the brain through the condition which in Amphioxus remains permanent as the adult brain.


As has been demonstrated by several recent investigators, the fore-brain and olfactory lobes are simple outgrowths of the dorsal wall of the thalamencephalon. They appear early in the development, it is true, but such early appearance is undoubtedly a coenogenetic phenomenon. That there is a substantial agreement between the Amphioxus brain, and the higher vertebrate brain of this stage, is perfectly evident. There is always a thalamocaele bounded anteriorly by a lamina terminalis to mark the boundary of the primitive end of the neural axis, and above, behind and on either side of this primitive lamina terminalis, the optic diverticula are given off from the brain.

D. All the setise organs developed in connection with the anterior end of the Amphioxus body are probably paired ; some of them certainly are, e.g. the eye-spot.

As I shall show in the next paragraph, the eye of Amphioxus exhibits unmistakable traces of bilateral symmetry and a tendency to develop into two pigmented areas in connection vrith diverticula of the thalamocosle, so that here 1 need only mention the fact, that I have been able to trace fibres from the olfactory organ through the walls of the olfactive diverticulum or bulbus olfactorius to both sides of the brain. Whatever this organ may prove to be, on further investigation of its ontogeny it is supplied from bilateral brain centres and affects both right and left co-ordinating tracts. The organs of special sense developed in the course of the two anterior pairs of nerves are certainly bilaterally symmetrical structures.

E. The eye-spot or eye of Amphioxus is the forerunner of the vertebrate eye, and shows traces of several stages in the development of the retina of higher forms. In itself it is not an organ of sight, but a light-perceiving organ.

After a careful study of the Amphioxus eye-spot, and related structures, I have become convinced that this animal presents us with the earliest stage in the phylogenetic development of the vertebrate eye.

As is well known, this eye-spot, which is considered a pigment spot, lies across the anterior end of the neural axis in the anterior end or wall of the brain, i.e. in the lamina terminalis, in an extended sense. It is not widely known, however, that this pigment spot assumes a large variety of shapes as well as positions, with respect to the anterior wall of the ventricle and to the first pair of cranial nerves. The most usual form is that of a slightly bilobed mass ; the lobes being placed to the right and left of the median line, so as to cover the roots of the first pair of cranial nerves more or less completely.

Other forms have been described by the various authors who have written upon the subject, and they are easily observable in any series of individuals. As already stated, the spot is very variable in size and shape, and its extremes may be set, as the convex or concave (forwards) lens shape, and the close grouping of most of the pigment cells in the wall of the lamina terminalis on the one hand, and the separation of the mass into three portions (two ventral and lateral, and one dorsal and median) with outlying scattered pigment cells on the other hand. These various forms grade insensibly into each other, and evidently depend in large degree, if not entirely, upon the mig^tory capabilities of the pigment cells in a state of nature.

These variations, then, are caused by the shifting of the pigment cells. It may be frequently observed that the two pigment masses pass out into the two nerves of the first pair. Where this modification occurs, it will be found associated with a pair of diverticula of the median ventricle which make their way out into the nerve roots. These diverticula are lined by the same cells that form the inner lining of the median ventricle, and the pigment cells lie among the cells of the second layer, or layer of percipient elements.

In this manner the light-perceiving organs are carried toward the surface at the ends of diverticula of the primitive brain cavity, reproducing in the phylogeny of Amphioxus the first steps of the series known for the remaining vertebrates.

We have only to think of these two pigmented optic structures brought into relation with the ectodermic structures — lens, cornea, etc., — of the higher vertebrate eye, in order to have all the steps of eye production carried out in Amphioxus. We know of no such relation of the ectoderm in the Amphioxus, and consequently conclude that, all facts considered, Amphioxus is descended from some ancestral form along with other vertebrates, but that, owing to its simple habits of life, has never required a lens or other focusing apparatus for the purpose of image perception, — simple light-perception sufficing for all its needs.

As Hatschek has shown, the pigment spot appears in the nervous layer long before the closure of the anterior neuropore One of the causes operating to transfer the pigment from the brain wall to the periphery is the constant growth, from the larva to the adult, and the consequent thickening and increasing opacity of the superjacent tissue.

After these diverticula have formed, there is left of the anterior brain wall between them a median portion which, as we shall see, is the homologue of the lamina terminalis of the remaining vertebrates.

The lamina terminalis of this stage contains the basis of the cerebral lobes, and the olfaclive centres of all the higher forms.

The relation of the parts here described corresponds with the facts as given in the latest and most accurate studios of vertebrate ontogeny from all classes of vertebrates, which form a valuable basis for the examination of this proposition from the comparative standpoint.

An examination of Hatschek's figures, 64, 6j, 67, and 69, for an explanation of the relation of the parts, shows that the most anterior portion of the neural plate of the young larva remains for a long time in its primitive flattened, uninclosed condition. Here the dorsal surface of the plate is still exposed to the direct action of external stimuli; its face is in or near the horizontal plane, and hence looks vertically, or nearly vertically, upwards. The eye-spot is developed in this area, and it clearly occupies the most favorable position for an important sense organ that the body of Amphioxus affords.

As the anterior neuropore closes up more and more, the anterior lip grows upward curving backwards, the pigment spot comes to lie in the vertical portion of the anterior end of the now completed canal ; consequently it is strictly terminal in its adult relations, but may, and frequently does, assume a position at the side and behind the end of the axis.

For greater functional power, the central (median) portion of the pigment spot has grown upwards (dorsad), and carrying with it a portion of the ventricular wall has produced the pineal eye.

Let us follow through the development of the nerve cord of the larval Amphioxus. Formed as a thickened plate of cells on the dorsal surface of the embryo, for a long time it lies open and exposed to the sea-water; its cells bear cilia which are doubtless sensitive to various stimuli. Long before the neural plate is converted into a cylinder (but only after the plate has been overgrown by the lip of the blastopore), pigment makes its appearance in some of the cells of the plate. At present we have no complete account of the appearance or early relations of this pigment matter; but the mass called the eye-spot appears shortly after the first mass which arises in the middle of the length of the plate, which at this stage falls in the fifth somite. The eye-spot soon becomes much more important than any of the posterior pigment-cell groups, and remains so throughout life. As already stated, it at first faces upward, but later acquires a facing at right angles to this* direction on account of the closure of the neuropore, the development of the head fin, and the gradual thickening of the tissue directly above the spot. Of course with this thickening of the body walls, more and more light is cut off from the spot, and the direction from which light reaches the spot in greatest abundance is from the front and sides of the head. The head fin fold divides the light falling upon the spot into two lateral bundles of rays, which, owing to less thickness of tissue through which they are compelled to pass, fall upon the sides of the spot with greater energy than light from any other source.

It is, then, owing to the relations of the external features of the head that the primitively median pigment body (not necessarily from an unpaired source) divides into two lateral portions, each of which strives to get nearer the surface, and in accomplishing the transposition cause an outgrowth of the brain wall, producing the two antero-lateral diverticula spoken of above.

The relation of the two diverticula to the bases of the first pair of nerves is of great interest in this connection, for, as we know, the surface of the head end of the body of Amphioxus — especially of the young — is pigmented along certain lines, over certain areas ; and it appears highly probable that the pigment cells of the surface have still some intimate relation to the light and heat perception, — one or both. The pigment of the central canal is derived from the pigment of the superficial ectoderm, which in the adult has nearly disappeared.


The primitive sense cells of the ectodenn transmitted through the nerve fibres of the first pair of nerves general impressions. from which those percipient elements of the brain associated with pigment cells selected vibrations of those wave lengths productive o{ the sensations of light and heat. The percipient elements not associated with pigment cells selected and were affected by only such stimuli as gave rise to other sensations, taste, smell, touch, etc.

Now that we have seen how most of the structural details of the brain form presented to us by all vertebrates higher than Amphioxus may have arisen out of the simple Amphioxus type, there remains for consideration a structure whose significance, both morphological and physiological, is still a matter of discussion, viz., the hypophysis. So far as I have been able to discover, there does not exist in Amphioxus the slightest trace of such an organ ; but it is not difficult to see how such a structure could arise from the ventral portion of the thalamoccele, in connection with the further development of the mouth and its sense organs. For the present I am not in position to say more of this structure, than that the hypophysis in Ammoccetes is intimately related with the olfactive area, and was probably an organ of taste.

We have then, in Amphioxus, all the stages in the development of the paired eyes of vertebrates (as well as of the pineal or unpaired eye) demanded by the theoretical considerations, save the final ones of the formation of the completed optic vesicles and lenses. The completion of these stages occurred somewhere in the phyletic series between the Amphioxus condition and the Cyclostome condition. In the Cyclostomata (Ammoccetes) the optic vesicles grow out only slowly, and after the animal has passed the Amphioxus stage.

It should not be forgotten that the optic vesicle, as it pushes out from the brain, presents its anterior hemisphere to the exterior ; and that in most vertebrates this half remains unpigmented, while it is this anterior portion which is pigmented in Amphioxus. Such must have been the primitive condition of the optic vesicle however developed.

From what has been said, it follows that there is no posterior hemisphere developed, because the process never goes far enough to form a spherical bulb, and an optic stalk.


That these difiFerences are due to primitiveness of the organs in Amphioxus, and not to any inherent fundamental differences between the eyes of Amphioxus and the corresponding parts in other vertebrates, will be apparent to any one who will analyze and compare the earliest stages in the development of the eye in the several vertebrate groups.

We cannot believe that the paired eyes of vertebrates, as they are known from the Cyclostomes upward, sprang into existence with complete optic vesicles, optic stalks and nerves. Much less, that they were provided from the first with lens and cornea ; on the contrary, the facts of ontogeny, the existence of such an idea as that of evolution in the domain of biological science, compel us to assume that the process was a gradual one and lasted through a long period of time, progressing only by minute increments, beginning with such a rudiment as I have shown to exist in Amphioxus. With the increase in complexity of organization of the type and specialization of the functions of the sense organs, came the added increments, which have resulted in the very complex, and in many ways still imknown, structure and relations of the paired and median eyes.

It is further unavoidable, that we conclude that the rudiments of eyes were functional from the very first or incipient stages through each modification up to the completed form, and that the physiological function of the organs in question have undergone as extensive, as important, and in every way a parallel growth, by slight increments acquired with the added morphological increments.

To those morphologists who object to the view I have thus briefly stated and endeavored to support, that such simple diverticula as are found in Amphioxus associated with pigment spots are entirely inadequate to give rise to such complicated structures as the eyes, I wish to give answer here : that we have in the case of the extremely complicated organ of the mammalian ear, an organ which has originated in a very similar manner, and whose every stage of development may be traced in existing vertebrates and about which morphologists are agreed that it is formed by simple involution of primitively superficial sense organs. The development of the cochlea, and its contained structures, is another instance of the production of an extremely complicated organ from a simple diverticulum pushed out from a previously existing cavity, — every stage of whose phylogcny lies before us in existing vertebrates.

The chief merits of the theory I have here attempted to establish is, that no demand is made upon the organism to supply any new structures, but simply to develop organs and structures already existing, in connection with a function of which we have evidence enough that all animals endeavor to acquire in ever increasing perfection, — i.e. light -percept ion and the possibilities which grow out of it.


F. The pigment of the ryc-s/>ot of Ampliioxus is contained in cells which normally lie inside the bounds of the nen-e mass, and whenever found outside in microscopical preparations, it is to be considered as misplaced by chemical or mechanical means.

Sections through the Amphioxus brain, prepared without contraction, or tearing, from well-preserved material, never show, so far as my experience goes, the free pigment granules lying in the interspace between the anterior end of brain and its sheath. This point is worthy of mention, since the presence of such free pigment particles has given rise to erroneous ideas as to the structure of the eye-spot, and the nature of the pigment deposit.


G. The pigment bodies of the central nervous system of Amphioxus are connected with, and form a part of segmental sensory structures.

These structures are doubtless derived from the superficial sense organs of that ancestral form in which the neural plate had not yet been converted into a tube, or had not received a protective covering.

As they exist in Amphioxus to-day, the regularity of their disposition is somewhat interfered with by the rearrangement of the cellular elements forming the bases of these structures, which are now transformed into a part of the central nervous apparatus. They consequently retain only indirect connection with the peripheryAfter the formation of the neural plate as an embryonic organ, the cells retain their embryonic condition for a varying length of time. The transformation of these cells into the elongated and greatly enlarged spherical, functionally active cells, occurs concomitantly with the development of the mesodermic somites and the peripheral sense organs.

This resting stage into which the cells of the medullary plate as a whole pass, as soon as the plate has been fully formed, illustrates the retardation of the development of the structure, and consequently function, of the apparatus, and this fully serves to explain why the superficial sensory organs and their pigment bodies remain undeveloped until the nervous system is entirely inclosed. For, although the medullary plate enters on a resting phase, the remaining organs of the body continue their development, especially the mesodermic structures, which by rapid growth inclose the nervous plate long before the resting phase has passed, and the differentiation of the permanent filM'es and ganglion cells of the nervous cord begins.

H. Each one of the pigment bodies is connected with^ forms a deposit in^ an amoeboid cell. All these cells retain their amoeboid nature throughout life, the pigment cells of the eye-spot not excluded.

The pigment-bearing cells are relatively large, being in the majority of cases equal to the middle size ganglion cells. The pigment makes its appearance in the cells of the growing larva in the form of particles of melanin, which may or may not fuse into a single mass. The particles are related in some unknown way to the protoplasmic structure of the cell, and are controlled by the cell, massed together in a more or less irregular lump in the contracted condition, or spread out in the form of threads, sheets, rows of particles, etc., in the expanded condition, of the cell.

The pigment cells arise bilaterally near the centre of the somites, and multiply in such a way that they take in more or less of the segment longitudinally. In the contracted condition the pigment frequently appears in the form of crescentic bodies, hemispherical cups, either simple or with rays streaming out from the periphery.

The nucleus of the cell is frequently visible, though the cell wall is usually hidden by the pigment.

The nucleus is eccentric in position and in carmine stains, it colors, with its cell, much like the ganglion cells with which it is associated.


According to Stieda, the general shape of the cells during life is that of an irregular star.

It is not at all difficult to find, in the preserved Amphioxus, cells with several pigment processes, and often the length of the processes exceeds twice the diameter of the central mass.


I. Tkt pipncnt of the axial nervous system of Amphioxus is in process of migration towards the anterior end of the body — towards the eye.

Where the eye is large, the interspace between it and the first pigment group is long, and vice versa. With the increasing opacity of the body walls, of the sheaths, and of the central nervous system itself, correlated with an increase in the degree of complexity and heightening of the function of the lightperceiving organs, the pigment cells scattered throughout the entire length of the neural axis migrate to the eye, and become associated with the percipient layer.

The interspace between the eye-spot and the first group of pigment bodies is dependent upon the size of the eye-spot — i.e. upon the sufficiency of its function for the body.

Stieda describes the pigment bodies as lying mostly in a plane passing horizontally through the ventral wall of the central canal; I find however that the cells oftentimes make their way dorsad along the walls of the canal, and may send processes outward from the canal reaching quite tn the periphery of the cord.


J. Rhode's conclusion that the giant ganglion cells of the anterior portion ef the spinal cord of Amphioxus send out axis cylinders only caudad is erroneous, and as my preparations show, Stieda's observations are correct both in figure and text.

Notwithstanding Rhode's positive assertion to the contrary, I am fully convinced that the giant ganglion cells show connec. tion by means of a plurality of axis<ylinders, with structures lying both caudad and cephalad of them.


K, The vertebrate ear lias developed within the phylum above Amphioxus, and arose from one of the primary sense organs of the lateral line system, at a period phylogenetically later than the formation of the canal system of these sense organs. The ear organ has retained in its inclosed state the tendencies of growth possessed by the surface organs y and in the vertebrates above the Ichthyopsida offers tfte only remnant of the perfected primitive canal system of sense organs.

The position of the ear capsule does not mark a divide between two morphologically different portions of the brain, nor has this capsule played any part in the formation of the brain contours.

No explanation has ever been offered of the origin of those peculiar structures, the semicircular canals, of which Foster says, " But the peculiar features of the semicircular canals suggest almost irresistibly that they are special agents " in the equilibration of the body.

The solution here offered makes clear why these canals are semicirculary and why they, as canals, have such special and morphologically significant relations to the sense organs in the ampullae, and it further helps us materially in forming a judgment as to the function of these organs which have so long proved a fruitful source of speculation, experiment, and difference of opinion.

Our knowledge of the development of the sense organs of the lateral line, and of the canal system, so intimately associated with them, we owe to several writers, but E. P. AUis has given us the most detailed and accurate account of these organs as they occur in Amia. Briefly stated, the steps of the developmental process are as follows: i. The layers of the ectoderm thicken over certain areas and sink below the general level of the surface of the body. These thickened bodies lie thus in the bottom of relatively extensive surface depressions of the general body surface. The ultimate sense organs are meanwhile forming, and as they do so each sinks below the bottom of its depression and lies in a pit, the lips of which soon grow upwards and inwards towards each other. By their coalescence they form an arch over the organ, which is soon converted into a canal, by the rapid growth of the edges of the arch away from the organ, and their fusion along the median line of the depression over which they arch as they grow.

Canals originating thus, continue to grow until they meet some other canal opening, or until the exhaustion of the impulse. In the former case the two terminal pores of the canal fuse into one ; in the latter the primitive canal possesses a strictly terminal opening. The sense organs, in the meantime, have become differentiated out of the indifferent epithelium, and present the appearance of a rounded elevation covered with hair or rodbearing sensory, columnar, epithelial cells.

The key to the solution of the whole problem lies in explaining the development of the internal ear on the basis of the development of the canal organs of the surface of the body.

When we examine the development of the canals and cochlea from the primary auditory vesicle, in the light of Allis' investigations, we find that the whole process consists in the further development within the head of one of the depressed areas and its sense organs, that are found in numbers on the body (head region) of all embryo vertebrates, and just as the primary sense organs of the surface of the body may (and usually do) produce several or many organs, so does the organ inclosed within the vesicular involution of the ear continue to multiply, until it has produced the constituent parts of the adult ear of a given vertebrate fonii.

Some of the deductions from these premises are as follows : —

a. Each natural group of vertebrates at the present day has a type of internal ear closely adhered to by all its members.

The so-called single semicircular canal of Myxine being, in reality, a double structure possessing two ampulla and ampullar sense organs, the homology of parts between Myxine and Petromyzou is essentially complete.

b. The semicircular canals, among the Elsamobranchs, many times show a condition of canal development, indicative of the fusion of the primary pores at the two ends of the same canal, with an incipient separation of the primary pore thus formed from the rest of the ear.

c. In any study of the functions of the internal ear, we cannot lose sight of primitive function of the sense organ giving rise to sunsory apparatus of the ear. For the functions have not suffL-red greater alterations than the structures, and there is no difficulty whatever in making out the structural relations of the primary and finished organs.

d. If the function of equilibration, as supposed, belongs in large part, or entirely, to the semicircular canals and their ampullar organs on account of their spatial relation's, we cannot overlook the fact that, among the lower vertebrate forms, canal organs are placed in much more favorable position (on the surface of the body) for the reception of stimuli than are the deeply buried ear canals ; besides which, the former lie further from the centre of motion, and would consequently execute greater excursions than the corresponding ear canals during any given motion of the body.

These surface canals occupy positions in the three planes of space just as the ear canals do.

e. Since from an extended consideration of the experimental evidence, derived from investigations of the function of brain and ear, with special reference to the function of equilibration, we find that the semicircular canals, and their organs, are not more directly connected with the centre of equilibration than many other sense organs, and other parts of the body not sensory in function, and since we know, from their history of development, that they were purely protective structures originally^ and have only had the semicircular form and spatial relations impressed upon them, as it seems, by the purely mechanical circumstances of involution, independently of any special function more than they possessed on the surface of the body, we must conclude that the semicircular canals have never^ and do not noWf possess any peculiar or special relation to the function of equilibration,

f The system of canal organs is a very ancient, and, so far as the existing vertebrates are concerned, a very primitive, system. Amphioxus apparently has no trace of it, but all other vertebrates show, by the possession of an internal ear with semicircular canals, etc., that their ancestors must have possessed a well-developed system of canal organs in the head region.

From this primitive condition the existing variety of forms of canal organs and other sensory structures of this class have been derived.

L. The higher sense organs of the Cyclostomata are all paired^ since the nose (i.e. the nasal or olf active epithelium) exists in the embryo as well as the adult in the form of two circumscribed areas lying on eitlier side of the median linCy each of which receives the entire nerve supply afforded by the olfactory nerve of its side.

It is evidently not consistent with our morphological ideas, to consider an organ unpaired and median when its eiitntiai structures are distinctly paired and bilaterally symmetrical, — even though some accessory portion has been so modified as to have lost all trace of its double origin. So far as I have discovered, the general acceptation has been that the Cyclostomea possessed only a single nasal organ, a single median olfactive area to which both of the olfactory nerves gave up their fibres. It is true, this supposed relation of two olfactory nerves to a single olfactive area has caused comment, and the explanation has been offered that we had to do with a modified condition, — a degradation of high sense organs. But as my sections show, the proximal portion of the nasal pit is divided by a median, nonolfactive raphe, into two lateral pockets, or rigkl and lefl nasal pits, to which alone the olfactory nerve of the right and left sides, respectively, are distributed. The median territory is supplied by branches from another nerve, which one I have not been able to determine specifically.

1 wish to call attention to the fact that, among the lower vertebrates there is a connection of the two olfactory pits across the median line by way of the mouth, here especially distinct, but among the higher forms it is also evident. This connection is usually brought about by means of grooves, placing the olfactive pit in communication with the mouth. Even in the mammalia the formation of a median partition to the extent of the formation of two nasal canals is a secondary process. The primitive or embryonic condition shows two simple pits, separated by a more or less distinct partition, which is usually a broad one. Of course in this stage the pits arc not deep, and by the time their boundary walls become extensive the median portion is also well developed. In Petromyzon the partition remains rudimentary.

I have, from my studies on Ammocortes and Petromyzon, ventured to make my statement a general one for the Cyclostotomata ; and I feel sure there is no reason to doubt that Myxine and Bdellostoma will be found to have their nasal apparatus, bilaterally symmetrical, with as great distinctness as Petromyzon shows this very important condition. The embryonic rudiment of the nasal pits in the earliest stages of epithelial differentiation, needs further study, as none of my stages arc young enough to prove that the olfactive areas arise entirely independently of each other, though I have no hesitation in venturing the prediction that this will be found to be the case.

M. The parietal-pineal eye of the Cyclostomata and other vertebrates has been developed from a median portion of the pigmented eye of Amphioxus. The rudiments of this eye were derived from (segmental^ sense organs^ but the eye itself is never developed from two right and left halves y in so far as the closure of the medullary folds would necessitate this.

No absolute demonstration of this view is at present possible, but I wish to offer the following considerations in support of it.

1. The parietal eye of vertebrates is formed as a hollow outgrowth of the anterior portion of the roof of the primitive thalamocoele, and its cells contain pigment.

2. The pigment contained within the cells of the bulbar, or functional portion of the pineal eye, is derived phylogenetically from the median portion of the pigment body of the anterior end of the primitive thalamoccele of an Amphioxus-like form.

3. The genetic connection of these three organs, for lightperception and sight, viz., the two lateral eyes and the median unpaired eye, is furthermore rendered probable by the central connection of all three organs, which is found to be in the optic thalami.

4. The same essential elements are present in eacn, — pigment cells and percipient rods and cones.

5. All three organs were formed to supply the demand for the restoration of the more perfect conditions for light-perception, destroyed by the folding in of the medullary canal.

6. The two kinds of eyes were primarily alike in structure and lensless; both formed lenses, the paired eyes first, — and this condition has been retained by all descendants, the pineal eye only in certain forms, — ancestors of the groups still showing traces of the lens body, and their descendants. The double nature of this organ, recently described in Leydig and Selenka, does not affect the above views, for, so far as we yet know (and the matter needs further investigation), both of the tubular outgrowths, although intimately related, are materially di£Ferent in one respect, viz., only one^ the epiphysis, contains pigment in its distal portion.

N. The neural axis of all vertebrates is co-extetisive with that of the cfiania, or vice versa, since the neural axis is phylogenetictdly as well as ontogenetically the older structure.

In this I can confirm Keibel's observation on raaramals, by my own on Sharks. The same is true o£ the early larval Cyclostomata and Amphioxus. My own results, the outcome of a study of Acanthias vulgaris and Galeus canis, at the Maine Biological Laboratory, Wood's Holl, Mass., were obtained several months before the publication of Dr. Keibel's paper. This relation of chorda and neural axis exists, not only in all the higher vertebrates, but in Amphioxus as well, during the stage in which the organs in question arrive at their complete separation from the surrounding tissues ; but while in higher vertebrates the notochord suffers a shortening of its anterior end, and not infrequently of its posterior end also, in Amphioxus the anterior end secondarily grows out into a process for the support of the pointed anterior end of the head.

A cephalic flexure occurs in both, and is more or less completely obliterated in both in the later stages, though from different causes.

In no craniate vertebrate does the notochord extend the entire length of the embryo when first formed, but ends in an undifferentiated mass of cells placed below and in front of the neural axis, and later grows out in front of it. This outgrowth is soon overcome by the much greater and more rapid growth of the brain. The conditions in Amphioxus are simpler in that the notochord is, from the first, distinct quite to the end of the neural axis, the anterior termination of the body being relatively much larger than in embryo of the higher vertebrata of corresponding stages.

O. Tlu pituitary prominence of the skulls of vertebrates does not mark a fixed point, as the relation of the anterior end of the chorda and of the hypophysial organs clearly proves.

I reserve a detailed consideration of this proposition for my illustrated publication.

P. In the discussion of the segmentation of the head it has become necessary to deny any segmental value whatsoever to any portion of the chondro, — or ossicranium. They have no greater segmental value than the intestine. And all apparent segmental characters have been impressed upon them by otiur organs of segmental nature. Not only does ontology force this conclusion^ but the historical development of our anatomical knowledge alike compels its admission.

It is taken for granted that the head region has been formed by a gradual process of modification of the anterior end of some ancestral type, whose body, with the exception of the first and last segment, was composed of nearly, if not quite, homodynamous segments. The problems are to determine what was the value of these primitive segments, and how they have been so modified as to produce the head. Obviously the only way oppn to the morphologist is to determine what existing vertebrates show the steps of this process, and the extent to which the primitive segmentation persists in the highly differentiated vertebrates of this age.

Few if any topics of vertebrate anatomy have received the attention of so many morphologists, or have been discussed with such interest, as the nature and development of the head.

It has long been recognized that within the vertebrate phylum the cephalon undergoes a most wonderful degree of differentiation, unequalled by any other portion of the body. As the lowest step in this series we have Amphioxus with the head less developed, both morphologically and physiologically, than many annelids and arthropods, — with this reservation of course, that in the Lancelet, as we say, the type is higher. From Amphioxus to the next stage, as represented by the Cyclostomes, the transitional forms are unknown, but the larval development of Petromyzon gives some interesting hints as to the manner in which these transitional stages have been passed through. From the Cyclostomes up to man, the series is practically unbroken, and allows us to trace, with a great degree of accuracy, the course of development, and to formulate some ideas as to the causes which have been at work effecting the progress.

Morphological conclusions, in the realm of neurology, have undergone great modification within the last decade, and as our knowledge increases we have found it necessary to widen our views as to what is normal and essential for a neural segment. From a general survey of the field, it is clear that a classification of the cephalic structures of modem vertebrates must be made, separating those which are genetically connected with the primitive organs, persisting with no change of function from those which have appeared much later and in a modified condition of the body. The brain is of the former class, the cranium of the latter. As an illustration, we may take the cases found in nature of a completely segmented vertebral column and its separation from the skull by an articulation, and the opposite condition of a continuous cartilaginous skeleton, including vertebral column and cranium. The explanation current is, that in the latter case we have to do with secondary fusion, and that we have here a modified condition derived from the typically segmented condition by a lack of development of the articulation. I consider it the true view, that a continuous cartilaginous skeleton has been, and is in some living cases, the primitive and normal condition, though of course I do not deny the production of more or less continuous portions of the skeleton by a process of secondary fusion.

The segmentation of the contained or enveloping organs does not predicate the segmentation of the containing or enveloping structure, any more than the formation of an ear capsule of a mammal, out of separate bones, predicates the segmentation of the sense organ contained.

Q. The luad cavities, or spaces included •within the mesoblastic somites occurring in tlie head region, possess relatively tlie greatest importance in an acraniate stage before a skull or anything comparable with a primordial cranium has made its appearance. This is tru£ from tlie ontogenetic as well as pkylogenetic standpoint.

R. The hypophysis is a structure which arose in the vertebrate phylum long after the chorda was established, as Amphioxus proves, and was connected in an important way with the infitndibulum. It arose as an organ of taste, and the infundibulum was its nerve.

S, The optic chiasm {the trochlear chiasm as well) has arisen within the vertebrate group above the Amphioxus condition and in the following manner: —

The fibres supplying the pigment spots (or muscle) arose from ganglion cells of the multipolar kind, and as we know in Amphioxus and Cyclostomes, these fibres cross the middle line not unfrequently, or the cells lie in the axial line of the nerve cord or brain. By a gradual process of development, it canie about that the majority of fibres for the right side of the body found their central ends in the left side of the brain, for some as yet unknown cause, although this transposition was probably intimately connected with the development of the system of association fibres.

T. The explanation of the increased number of gill slits of Amphioxus over those of other vertebrates {which certainly show traces of considerable reduction in number) is to be found in the habits of the Amphioxus ^ which is not a free swimming animal^ and cannot be a predatory one. It depends^ for its foody upon the size and power of its branchial apparatus to create currents and keep moving a sufficient volume of water to supply it with the requisite amount of foody which is contained in only limited quantities therein.

As the animal grows larger its needs are greater ; the branchial chamber and apparatus must increase to allow a larger volume of water to pass.

U. The branchial apparatus of Amphioxus is then not merely a respiratory apparatus, but more an apparatus for the collection of food and for the transfer of such collected store to the pharyngeal opening for deglutition. A much smaller organ than the branchial basket of the adult animal would suffice for the adequate respiration.

We have only to call to mind the peculiarly inactive life that the animal leads, to become satisfied that its so-called respiratory apparatus is much more important as a food collector and strainer than as a respiration organ.

This modification of the branchial apparatus, for food collection, is paralleled in higher vertebrate by the production of mandibulo-maxillary region for the same piupose.

The Lake Laboratory, Milwaukee, Wis. April 21, 1890.



Cite this page: Hill, M.A. (2020, August 4) Embryology Paper - Vertebrate cephalogenesis 1 (1890). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Vertebrate_cephalogenesis_1_(1890)

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