Paper - The development of the auditory nerve in vertebrates

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Cameron J. and Milligan W. The development of the auditory nerve in vertebrates. (1910) J Anat Physiol. 44(Pt 2): 111-32. PubMed 17232833

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This 1910 paper by Cameron and Milligan is a historic description of auditory nerve development in a number of species including frog and lumpfish (Cyclopterus lumpus).

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The Development of the Auditory Nerve in Vertebrates

By JOHN CAMERON, M.D.,D.SC., Department on Anatomy, Middlesex Hospital Medical School;

and

WILLIAM MILLIGAN, M.D., Lecturer on Diseases of the Ear, University of Manchester, Aurist and Laryngologist to the Royal Infirmary Manchester.


I. Introductory

In 1906 the authors read a paper before the Otological Society of the United Kingdom on the development of the auditory nerve, founded on a study of the embryos of a few vertebrate types (5). This was meant to partake of the nature of a preliminary communication, as it was deemed advisable to secure material representing all the great vertebrate classes before embarking upon a more pretentious publication. The work has been considerably delayed owing to the difficulty Which Was experienced in obtaining a supply of representative embryos. This hindrance has, however, been of service in permitting us to make an extensive comparative study of the developing auditory nerve throughout vertebrates.


It may be stated at the very outset that our results afibrd unequivocal support to the multicellular theory of nerve genesis. Evidence in support of this theory has been previously advanced by one of us in the case of the optic nerve (8) and the spinal nerves (10). The conclusions arrived at as a consequence of the present investigation are thus confirmatory of these previous observations. The auditory nerve was chosen for the purpose of the present research for two reasons. With the view, firstly, of ascertaining embryologically the mode of continuity of the fibres of this nerve with the sense-epithelium on the one hand, and the cells in the nuclei of the hind brain on the other. The second reason for choosing the auditory nerve was, that it affords a favourable opportunity for investigating the question of nerve histogenesis, as in this case the end organ and the central nervous system are in close association with one another from the early developmental stages.


Methods. — The embryos were fixed in Bles’ fluid, and cut transversely to their long axes. The sections thus produced were mounted serially, and subsequently stained on the slides. After several experiments it was ascertained that the iron-alum-haematoxylin method of Heidenhain, slightly modified, demonstrated the nerve fibrils to the most favourable degree, and this was finally chosen as the chief colouring agent. The achromatic and chromatised phases of the primitive axis cylinders, to be referred to in the subsequent description, were found to be very clearly defined by this mode of staining.

II. The Auditory Syncytium

The earliest rudiment of the auditory nerve consists of a large mass of cells developed from the cephalic portion of the neural crest. This is termed the facial-acoustic ganglion (or complex of American authors), which early divides into its component elements, the facial portion forming of course the geniculate ganglion. The auditory portion takes up its position between the hind brain and the developing otic vesicle. We made a series of reconstructions of the latter in the various vertebrate types examined, and found that the ganglion rudiment became applied to it in such a way as to come into intimate relationship with, on an average, about one-third of its superficial area (figs. 1 and 2). A further study of this relationship in the more advanced stages brought into prominence the interesting fact that this is the only portion of the wall of the otic vesicle from which the special sense-epithelium is derived, the cells of the remainder undergoing retrogression and flattening to form the characteristic arrangement seen in the adult. This area, which will be hereinafter referred to as the sense-epithelium patch, .exhibits active karyokinesis, so that it is evidently destined to form the essential auditory cell-elements of the membranous labyrinth.


On turning to an examination of the auditory ganglion itself by high powers of the microscope (,1; and 1% , it could be clearly established in all the vertebrate types that, at a certain stage, this consisted of a mass of nuclei imbedded in an apparently structureless and comparatively achromatic cytoplasm. The latter was readily traceable through the incomplete membrana limitans externa of the hind brain with the scanty cytoplasm of the neuroblasts there (fig. 3), ‘and, on the other hand, with the rudiments of the sense-epithelium in the otic vesicle through its equally imperfect membrana limitans externa (fig. 4). It is obvious, then, that the cell elements in the sense-epithelium patch of the otic vesicle are brought into close association with those of the hind brain in early embryonic life by a continuous tract of nucleated cytoplasm (fig. 5). The only title by which one can adequately denote the latter is syncytium. We have therefore decided to adopt this term in place of “ ganglion ” for the early stages of development. This decision is still further justified by the fact that the cells -of the spiral ganglion and the ganglion of Scarpa represent a quite insignificant proportion of those constituting the acoustic ganglion, as will be indicated in the subsequent description.

CameronMilligan1910 fig01.jpg CameronMilligan1910 fig02.jpg
Fig. 1. The relationship of the auditory syncytium to the hind brain and otic vesicle in a frog embryo of 8 mm. Fig. 2. A neighbouring section to fig. 1, showing the relationship of the auditory syncytium to the otic vesicle.


This intimate connection of the otic vesicle With the hind brain in the early phases of development is in close agreement With the observations of Graham Kerr on the motor nerves of Lcpidosiren embryos (14). This authority describes the existence of a protoplasmic “ bridge ” between the spinal cord and the myotome, which becomes fibrillated later to form the motor tract between the central nervous system and the end organ. This is the crux of the whole question of nerve genesis. The upholders of the unicellular theory of nerve origin have undoubtedly been misled through a failure to recognise the existence of this bridge. The latter was certainly prominent in the case of the spinal nerves of frog and chick embryos studied by one of us (10), and also in the optic nerve of frog embryos (8). Indeed, the term syncytium might be applied to the appearance presented by the nerve in the latter instances just as appropriately as in the case of the auditory nerve. We would venture to suggest at this stage that the full recognition of the syncytial phase of nerve histogenesis means the abandonment of the unicellular theory in favour of the multicellular.

CameronMilligan1910 fig03.jpg CameronMilligan1910 fig04.jpg
Fig. 3. Junction of the auditory syncytium with the wall of the hind brain in an 8 mm frog embryo. Fig. 4. Junction of the auditory syncytium with the wall of the otic vesicle in an 8 mm frog embryo.


This view of primitive nerve structure is likewise in close accord with those of Bethe (4) and (5), Apathy (1) and (2), Fragnito (11), and Schultze (20). It is also significant to point out at this stage that Sedgwick (21) some years ago drew attention to the fact that the developing tissues of the embryo are connected together by a continuous reticulum. Thus he showed that the neuroblasts of the neural tube are in direct continuity with the cell-elements‘ of the surrounding mesoblast through the medium of this network. Sedgwick’s work was adversely criticised at the time; but we have no hesitation in placing our seal on the accuracy of his observations. A good deal of the trouble has arisen from embryologists having insisted for years on the three-layered condition of the early embryo. After all, the mesoblast is really derived from the epiblast and hypoblast, We consider that it is much more accurate to regard the embryo as a homogeneous whole, somewhat after the idea of Sedgwick. More recently still, Bernard (3) has demonstrated that the cell-elements of the retina, not only those belonging to one layer, but also those of neighbouring layers, are brought into close. association with one another by means of a system of delicate interconnecting fibrils. To this he gives the name of protomitomic system.


CameronMilligan1910 fig05.jpg

Fig. 5. The continuity of the peripheral auditory tract in a 13 mm frog embryo.

III. The Further Elaboration on the Auditory Syncytium

The description of the mode of development of the auditory nerve in text-books of embryology is very brief. So far as one can gather, the main purport is to the effect that the cells of the acoustic ganglion become divided up in some mysterious way into two groups which ultimately become the constituent elements of the spiral ganglion and the ganglion of Scarpa on the cochlear and vestibular divisions of the nerve. The ganglion cells are afterwards described as giving ofl central and peripheral axis, cylinder processes which pass to the cells of the hind brain and the developing sense-epithelium respectively.


Our results are opposed to this current view of the mode of development of the auditory nerve. It will be recognised at the very outset that the commonly accepted interpretation of what takes place obviously does not explain the division of the ganglionic mass into its two main elements, seeing that the latter operation occurs previous to the development of the fully formed axis cylinders. The real explanation is found in a further study of the developing otic vesicle. The latter rapidly expands in surface area during the early stages, and very soon becomes constricted off into the utricle and saccule. This constriction passes through the senseepithelium patch of the vesicle and divides it into two portions, each of which bears away the part of the auditory syncytium attached to it. The division of the latter is thus brought about by the fact that the end organ and hind brain must have been previously in intimate association with one another through the medium of the syncytium.


We studied this splitting up of the auditory syncytium first of all in fish embryos, as in these the otic vesicle does not undergo the degree of elaboration found in higher vertebrates. A favourable opportunity was thus afforded of observing the exact relationship which the syncytium bears to the sense-epithelium patch of the otic vesicle.


CameronMilligan1910 fig06-10.jpg

Figs. 6, 7, 8, 9 and 10 are camera, lucida tracings of the otic vesicle and auditory syncytium of an embryo of Oyclopterus lumpus, a teleost.

They represent Nos. 96, 98, 100, 102, and 104 of a series of transverse sections, numbered from the cephalic end. The syncytium, which is coloured red, will be observed in fig. 6 (section No. 96) to correspond in size with the thickened sense epithelium patch of the otic vesicle, with the cell-elements of which it is in intimate relationship. In fig. 7 (section No. 98) the patch has divided into two areas, with a thinned portion of the vesicle wall between, and so likewise has the syncytium; the result being that the latter is still maintaining its close association with both. In figs. 8 and 9 (sections Nos. 100 and 102) the two sense-epithelium patches are still seen, whilst the attachment of the syncytium to the wall of the hind brain is likewise clearly indicated. In fig. 10 (section No. 104) the two patches have become completely separated, but the syncytium is preserving its intimate attachment to both. In the same figure a third patch has made its appearance on the semicircular canal in the lower part of the labyrinth, and it, in its turn, is in close association with an offshoot from the main syncytial mass. From a further examination of embryos of Cyclopterus lumpus it was ascertained that these subsidiary sense-epithelium patches were all derivatives of the originally single area, with which the auditory syncytium was in continuity during the early developmental stages (fig. 11).

CameronMilligan1910 fig11.jpg

Fig. 11. Diagram to show the relation of the auditory syncytium to the hind brain and otic vesicle in an early vertebrate embryo.


We consider that these above observations, which were confirmed by a study of the otic vesicle in embryos representing the higher vertebrate classes as well, clearly established the fact that the breaking up of the auditory gaiiglioii” is a necessary acconipaninient of the process of resolution of the sense-epithelium patch into its various component macular areas. Inasmuch as the latter are many as six in higher inammals, it follows that the syncytium must likewise divide into a similar number of links connecting these with the hind brain, and constituting the developmental divisions of the auditory nerve. Thus an examination of the otic Vesicle oi’ teleostean fishes revealed the fact that the primary sense-epithelium patch divided into areas for each of the three semicircular canals, the two maculze of the utricle, the saccule, and the patch at the remainder of the cochlea being quite rudimentary. The auditory syncytium followed suit, and resolved into a corresponding number of component parts, ‘ix’. seven in all 12). On investigating the condition in amphibians, we found that the sense-epithelium patch of the otic vesicle divided into areas for the three semicircular canals, the two maculie of the utricle, the macula of the saccule, and the patches for the cochlear canal and lagena. Each of these, as usual, bore away with it a portion of the syncytium, which thus became subdivided into eight portions (fig. 13).


In birds a process similar to that in amphibians was found to take place, our observations on embryos of this class of vertebrates confirining the description in a recently published book on the development of the chick by Lillie (17). Thus on page 295 that author states that “the acoustic ganglion from which the auditory nerve arises, takes its origin from the acoustico—facialis ganglioii which lies in front of and below the centre of the auditory pit. During the closure of the latter the acoustic ganglion becomes fused with part of the Wall of the otocyst in such a Way that it becomes impossible to tell in ordinary sections where the epithelial cells leave off and the ganglion cells begin. This fused area may be called the auditory neuro-epithelium. The neuro-epithelium is the source of all the sensory areas, which arise from it by growth and subdivision. The branching of the auditory nerve follows the subdivision of the neuroepithelium.




fiG. 12.—Diagram to show the seven areas into which the sense-epithelium patch of the otic vesicle divides in higher fishes, as also the corresponding subdivisions of the auditory nerve with their ganglia.



fiG. 13. —Diagram to show the eight areas into which the sense—epithelium patch of the otic vesicle divides in amphibians and birds, as also the corresponding subdivisions of the auditory nerve with their associated ganglia.


On studying the question in embryos of mammals, including man, the sense-epithelium patch of the otic vesicle was as usual observed to be in intimate association with the auditory syncytium. The former, as development proceeded, resolved into six areas for the semicircular canals, the utricle, saccule, and cochlea. Simultaneously with this, the auditory syncytium l)ccame broken up into six corresponding parts each of which remained in continuity with that portion of the otic Vesicle wall it was originally in association with 14). It was particularly interesting to study the way in which the developing cochlear canal dragged off its quotum of the syncytium with it. As the canal elongated and became coiled on itself, so also the syncytium was compelled to do likewise. The development of the auditory nerve in man has been so well described recently by Streeter (22) that we do not propose to enter into any further details here. We will refer further to this observer’s work in section V. of this paper. From the foregoing remarks it follows that it is obviously inaccurate to describe the auditory ganglionic mass as consisting of cochlear and vestibular portions, since these are not the fundamental elements of the nerve, however convenient these terms may appear when considered from the point of view of their physiology.


fig. 14. Diagram to show the six areas into which the sense-epithelium patch of the otic vesicle divides in higher mammals, as also the correspomling subdivisions of the auditory nerve with their associated ganglia.


His (12) described the nerves to the saccule and posterior semicircular canal as being derived in the human embryo from the cochlear division of the auditory ganglion. Certainly the arrangement of the foramina in the lamina cribrosa of the internal auditory meatus would lead one to infer that this view was correct. For example, the nerves to the cochlea and those to the saccule and posterior semicircular canal all pass through below the falciform crest, whilst those for the superior andexternal canals and the utricle make their exit above the crest. Streeter (22), however, pointed out that the filaments to the saccule and posterior canal are not developed from the cochlear division of the auditory nerve, but are derived from a portion of the ganglionic mass which forms the vestibular division.


The arrangement of the foramina in the lamina cribrosa in man is readily explained by studying the relative positions of the sense-epithelium patches on the membranous labyrinth. Such an examination will show that the macula of the utricle and the ampullae of the superior and external semicircular canals are close together, and therefore the nerves to these all pass through the area cribrosa superior. On the other hand, the macula of the saccule and the ampulla of the posterior canal are placed at a lower level and also much further apart, relatively speaking, so that the nerve filaments to these traverse the area cribrosa media and the foramen singulare, which are likewise separated by a slight interval.

IV. The α-, β-, dnd γ-Neuroblasts of the Auditory Syncytium and Nerve

The existence during embryonic life of three types of neuroblasts in the central nervous system has been demonstrated in a recent paper (9). These make their appearance in a definite order and represent distinct phases in the ontogeny of the nerve cell. To those met with in the earliest stages the term a—neuroblast was given. These undergo varying degrees of elaboration during the later phases, so that one can then distinguish two subvarieties, to which the terms ,8- and y-neuroblasts were applied. Of these the latter are readily distinguishable by the greater metabolic activity of their nuclei. They become invested by a considerable cytoplasmic envelope and thus develop into the nerve cells of such important regions as the sensori—motor areas, the cornua of the spinal cord, etc. The B-neuroblasts do not attain to such a degree of development, their cytoplasmic investment is relatively scanty, and they occupy a position subsidiary to the y-variety, both structurally and physiologically.

The α-, β-, dnd γ-types of neuroblast could be readily identified in the developing auditory ganglion. In the early phases the primitive ct-type is, of course, the only representative. Their nuclei were found to exhibit evidences of metabolic activity similar to those previously described for neuroblasts in other parts of the developing nervous system. The most remarkable sign of this metabolism in amphibian and fish embryos consisted in the ingestion by their nuclei of the particles of yolk with which the tissues are loaded during the early developmental stages. This was found to occur exactly after the manner adopted by neuroblast nuclei in other parts of the central nervous system of these lower vertebrate types. The existence of the “ assimilative pole” of these nuclei (9) could be readily demonstrated, and in most cases this was the one directed towards the otic vesicle (figs. 3 and 4). A further expression of the activity of these nuclei was to be found in the products of their metabolism. Their cytoplasmic investment in the early stages is very scanty, in fact so much so that it is often difficult to «convince oneself of its existence. Very soon, however, they become surrounded by a clear and almost achromatic envelope, a considerable proportion of which is nuclear in origin. This gradually increases in bulk and blends with similar material surrounding neighbouring nuclei. The performance of this “ achromatin function” by these neuroblast nuclei has been, previously described (9), so that it is not intended to dilate further on this subject here. It will now be recognised that the auditory syncytium is brought into being by the blending of this new achromatic material to form one continuous nucleated mass uniting the cell-elements of the otic vesicle with those of the hind‘ brain. We consider that the amount of perinuclear substance is not sufficient in amount to warrant the application of the term syncytium to the earliest developmental phases of the facial-acoustic ganglion.


fiG. 15. —The direction of the plane of mitosis in the auditory syncytium of a. rabbit embryo.


A third index of the activity of the nuclei of the auditory syncytium is "afforded by the remarkably free karyokinesis which they exhibit. This has been previously shown (10) to be one of the earliest signs of the development of the spinal nerves, and it is a rather interesting coincidence that it should also be prominently displayed in the case of the auditory nerve. Moreover, the plane of division always occurs at right angles to the line of the future nerve, as in the previous instances (fig. 15). r The result of this active mitosis is to produce a great increase in the number of cell-elements constituting the syncytium.


The further life-history of the a-neuroblasts, of which the auditory syncytium is composed, will be found to display certain interesting features. As development proceeds one can readily recognise a gradual evolution of the ,8- and y-neuroblasts from the primitive type.


fiG. 16.——fibrillation of the peripheral end of the auditory syncytium in a 13-mm. frog embryo.

The y-type will be readily recognised in three situations, namely, in the hind brain, in the wall of the otic vesicle, and in the syncytium midway between these points. Those in the wall of the otic vesicle form the senseepithelium, a better name for which is neuro-epithelium. These latter cells must be regarded as neuroblasts of the highly evolved y-type. They certainly satisfy all the requirements of this qualification. . Thus the nuclei are large and spherical in the resting condition, whilst the cytoplasmic investment is abundant, and exhibits fine fibrillae. The latter are continuous with the fibrillae which develop in the distal portion of the auditory nerve (fig. 16). _


The y-neuroblasts which tmake their appearance in the middle of the syncytial bridge form the ganglia associated with the cochlear and vestibular roots * of the auditory nerve. They constitute a very small proportion of the neuroblasts of the original syncytium. The fibrillae which develop in their cytoplasm are continuous with those in the proximal and distal portions of the nerve. It will, however, be pointed out presently that the latter are not formed from these neuroblasts, but are independent formations in the previously undifferentiated syncytial mass (fig. 17). The y-neuroblasts which develop in the central end of the syncytium form a large proportion of the nuclei of origin of the cochlear nerve fibres.


Their cytoplasm is abundant, as usual, and comes to possess delicate fibrillae continuous with those laid down in the syncytium (fig. 18).

The β-neuroblasts represent by far the greater proportion of those originally constituting the auditory syncytium, and will be found prominently displayed along the Whole course of the auditory nerve. Their nuclei are small, oval in outline, and are applied along the line of the nerve fibres (figs. 17 and 20). One has little difficulty in recognising that the β-neuroblasts become the cells of the nerve sheath and thus assume a position subsidiary to those of the -y-type, both developmentally and functionally.


fiG. 17. The fibrillation of the intermediate portion of the auditory syncytiumin a 13-mm. frog embryo. g Note also the diflerentiation of the 3- and -y-neuroblasts.


V. The Nascent and the Mature Phases of the Auditory Nerve—Axons

It has been previously pointed out that one can recognise a nascent or achromatic and a mature or chromatised ‘phase in the life-history of the axons of the spinal nerves (10). The material which is laid down along the path of the future nerve is at first quite homogeneous and undifferentiated, and thus merits the title of achromatic. It ought to be noted however, that the latter term is applied merely in a comparative sense. The mature or chromatised phase in the spinal nerves was shown to be produced by a peculiar chemical alteration in the above material whereby it became affected in a definite manner by staining agents. Treatment by the latter exhibited the existence of a fine longitudinal fibrillation which manifested itself simultaneously along the whole length of the nerve tract. To this profound alteration the term “ chromatisation ” was applied.


fiG. 18. —fibrilla.tion of the central end of the auditory syncytium in a. 13-mm. frog embryo.


We find that an exactly analogous change takes place in the case of the auditory nerve. Thus the previously undifferentiated cytoplasm of the syncytium becomes fibrillated simultaneously at all points of its course. Further, this important change occurs at the same time that the fibrillae are being laid down in the cytoplasm of the y—neuroblasts (fig. 17). Not only so, but the primitive fibrillae -may be readily traced along the whole auditory nerve tract, particularly in lower vertebrates (e.g. amphibian embryos); whilst their continuity with the neuro—fibrillae of the y—neuroblasts in the hind brain with those in the middle of the tract and with those of the neuro—epithelium can be freely established. This simultaneous appearance of the fibrillae shows that they are not developed independently of the syncytium as central and peripheral processes from the ganglion cells in the middle of the nerve, which is the usually accepted view of their mode of formation. Each fibrilla is exceedingly fine. Our impression is that the future axon is at first represented by a single one of these, the remaining constituents being subsequently laid down by further processes of chromatisation. The unit of nerve structure is, from this standpoint, not the axis-cylinder, but the fibrilla. We have certainly been unable to detect an outgrowth of fully developed axons from the cells of the acoustic ganglion to form the central and peripheral processes of the auditory nerve.


Unfortunately, our material was not in a sufiiciently good condition to permit us to make any definite statement with reference to the process of fibrillation in the auditory nerve of the human embryo. Wle were enabled, however, to gather that the auditory syncytium, with its undifferentiated cytoplasm, is as prominent in the human subject as it is in lower vertebrate types. In this relationship it is interesting to quote Streeter’s recent observations (22) on the developmentof the fibres of the auditory nerve in the human embryo. Thus he states1 that “in the embryos studied the proximal end of the nerve (cochlear nerve) could be made out almost as soon the distal. So it is possible that the cochlear trunk consists originally of a column of ganglion cells connecting the anlage of the spiral ganglion with the brain, and the conversion of this column into fibroblasts produces the early fibres of the trunk; this would explain the abrupt appearance of the nerve trunk in all parts of its course at once.” Streeter’s conclusions with regard to the origin of the axis-cylinders of the auditory nerve in the human embryo thus evidently agree with our own results for lower vertebrate types. He was apparently much impressed by the development of the fibrillae simultaneously along the whole course of the nerve tract, and we are glad to be enabled to confirm his suggestions regarding the real nature of neurogenesis. Streeter’s application of the te1'111fib1°0blcLst.9 to certain of the cell—ele1nents in the auditory complex appears to us rather felicitous. It will be recognised that these correspond to the ,8-neuroblasts described by us.


The cytoplasm of the auditory syncytium does not become wholly transformed into fibrils. The latter become congregated into groups to form axis-cylinders, the undifferentiated portion of the cytoplasm surrounding these persisting as the medullary sheath. The ,8—neuroblasts are, of course, the precursors of the cells constituting the neurilemma.

VI. The “Vulnerable Point” of the Auditory Nerve

That portion of the auditory syncytium which is situated next to the hind brain undergoes a rather interesting alteration during development. In this region the nuclei are very scanty, and the cytoplasm does not on that account appear to increase in amount, seeing that it is in some measure a derivative of nuclear activity. The result is that as the syncytial bridge gradually lengthens owing to the continued growth of the tissues, this portion becomes attenuated, and quite free from [3—neuroblasts (fig. 18). Indeed, by the time fibrillation occurs its calibre has become decidedly less than that of the remainder of the syncytium. The portion of the cytoplasm in this region which does not become differentiated into fibrils persists as the medullary sheath. Note, however, that since there are no ,8-neuroblasts left in this segment of the nerve tract, there can be no development of a neurilemma sheath. This explains why the latter terminates just before the auditory nerve enters the hind brain. Owing to this deficiency in the covering of the fibres, it is obvious that this segment must constitute a weak spot in the nerve trunk. In this relationship it is rather significant to study the results of Orr and Rows (18) on the lymphogenic origin of toxic infection of the central nervous system. These observers have demonstrated that, both in the spinal and cranial nerves in general paralysis and other nervous affections, the degeneration commences in the sensory roots just before they enter the central nervous system, that is, exactly at the point where they lose their neurilemma sheath. Orr and Rows have likewise found that, after the implantation of celluloid capsules containing toxins in various parts of the body, the resulting degeneration of the sensory fibres invariably started at this situation. They have accordingly termed this the “vulnerable point”; and there can be no doubt that it is so, considered from a developmental standpoint as well. fig. 18, which is drawn from a frog embryo, exhibits the early phase of fibrillation of the auditory syncytium at its junction with the hind brain. Note the degree of attenuation of this segment and its freedom from nuclei. It is clear from the foregoing results that the neurilemma sheath exercises an important protective as well as a nutritive influence over nerve fibres.


Turning now to the study of the distal end of the developing auditory nerve, it is found that an exactly similar alteration takes place there. Just before the syncytium passes through the external limiting membrane of the otic vesicle to become continuous with the cytoplasm of the neuro-epithelium, it becomes attenuated (fig. 16) and also freed from the nuclei of the B-neuroblasts in a manner similar to that Which occurs at the central end of the nerve. The cytoplasm of the syncytial bridge in this region becomes fibrillated as usual, and that Which remains undifferentiated forms the medullary sheath. Here, as at the central end, the deficiency of neurilemma sheath is explained by the absence of ,8-neuroblasts. It is therefore obvious that this segment of the auditory nerve is likewise Weak and unguarded, so that no doubt toxins would find a ready entrance at this point as well.



fiG. 19. The continuity of the ripheral auditory tract in a young frog.

Note the 7-neuroblasts of t e auditory ganglion. The hairs of the sense-epithelium are visible.



VII. The Mode of Continuity of the Auditory Sense-Epithelium with the Nuclei in the Hind Brain

We have already pointed out that the auditory syncytium, the yneuroblasts in the hind brain, the neuro-epithelium and the y-neuroblasts in the middle of the syncytial tract, become fibrillated simultaneously. The resulting neuro-fibrillae thus form one continuous bond‘ of union between the neuro-epithelium and the hind brain, This conclusion is in direct antagonism to the usually accepted view of continuity of the peripheral auditory tract. Thus Retzius (19), Lenhossék (15), Katz (13) and others have shown, by means of the Golgi method, that the peripheral and central fibres of the auditory nerve end in arborisations round the neuro-epithelium and the cells in the hind brain respectively. It is surprising to note how readily the appearances presented by Golgi preparations of the central nervous system have been accepted by histologists Without question or comment. Our results with this method on nerve endings have not been convincing enough to Warrant our placing implicit confidence in its use. Its action on embryonic tissues is undoubtedly very disappointing. The iron-alum-haematoxylin method is, to our Way of thinking, much more satisfactory and more immune from ambiguity in the interpretation of the appearances presented by the tissues. Certainly, in the embryos of vertebrates below the rank of man, this mode of staining demonstrates not a contiguity by synapse but a direct anatomical continuity of the peripheral auditory tract. Of course it is possible that the conditions which prevail during embryonic life may become profoundly modified by the time full maturity has been attained; but our investigations on more mature tissues by the iron-alum-haematoxylin stain have so far convinced us that this is not so. We have therefore decided to abandon the “idea of a synapse in favour of that of a direct anatomical continuity of tissue. Thus the intimate association which the auditory end organ bears to the hind brain during the early stages through the medium of the auditory syncytium never really becomes severed (figs. 5 and 19).


fiG. 20.—The auditory ganglion and nerve and the hind brain of a. young frog. Note the -y-neuroblasts of the ganglion and hind brain and the B-neuroblasts of the nerve.



VIII. Summary

  1. The auditory end organ is brought into direct anatomical continuity with the hind brain by means of a nucleated tract of cytoplasm to which the authors have applied the term syneytrimn.
  2. The breaking up of the auditory nerve into its various divisions is a necessary accompaniment of the differentiation of the wall of the otic vesicle into the various sense-epithelium patches, since each of the latter bears off its quotum of the auditory syncytium with which it was originally in intimate continuity. Thus the cochlear and vestibular portions of the auditory nerve are not its fundamental divisions. The latter are six in man, composed of one for each semicircular canal, one for the utricle, one for the saccule, and one for the cochlea.
  3. Three types of neuroblasts may be identified in the auditory syncytium. The term α-neuroblast has been adopted for those existing during the early stages.
  4. The β- and γ-neuroblasts are further elaborations of the α-type, and represent distinct phases in the ontogeny of the nerve cell.
  5. The γ-neuroblasts make their appearance in three situations, namely, in the hind brain, in the Wall of the otic vesicle, and in the syncytial tract midway between these points.
  6. The β-neuroblasts become the cells of the neurilennna sheath of the auditory nerve.
  7. The cytoplasm of the auditory syncytium is undifferentiated during the early stages. This represents the nascent or achromatic phase of the auditory nerve axons.
  8. This material becomes fibrillated longitudinally in a definite manner to form one continuous tract of neuro-fibrillae uniting the neuro-epithelium with the cells in the hind brain. This represents the mature or chromatised phase of the auditory nerve axons.
  9. The latter are thus not unicellular but multicellular in origin.
  10. Each axon is probably represented at first by a single fibrilla. The unit of nerve structure is therefore 11ot the axon but the fibrilla. ’
  11. Those portions of the auditory syncytium next to the hind brain and the otic vesicle become deprived of ,8-neuroblasts, and as a result there is no development of a neurilemma sheath at these points. The latter obviously represent sources of Weakness, at which toxins may readily find an entrance, as already shown by Orr and Rows.
  12. The intimate association which the end organ bears to the hind brain during the early stages through the medium of the auditory syncytium never really becomes severed. We have therefore decided to abandon the idea of contiguity by synapse in favour of a direct anatomical continuity of the peripheral auditory tract.

Addendum

Since the above was written We have received a printed notice of the forthcoming publication of a book by Professor Hans Held on Die Eiitwic/colmig dos Ncrveizgewebes bei den Wii°b(%ltioi"en. This circular is very brief, but is sufficient to enable us to gather that Held’s conclusions are entirely in favour of the multicellular theory of neurogenesis. The concluding words are very significant: “Nicht als eine Summe von Neuronen (VValdeyer), den ‘anatomisch wie genetisch getrennten N erveneinheiten,’ ist das Nervensystem entwickelt Worden, sondern als ein Neurencytium.” Held has adopted the Word nearenoytimn to denote the nucleated mass of cytoplasm to which we have applied the term synoytium, and has emphasised the importance of recognising this critical phase of nerve formation. We are glad to observe that our results on nerve histogenesis as studied in the auditory nerve are confirmed by the contemporaneous Work of Held.

Literature

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(18) ORR, 1)., and Rows, R. G., “A Clinical and Experimental Investigation into the Lymphogenous Origin of Toxic Infection of the Central Nervous System, Rev. Near. and Psg/ch., May 1907.

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