Book - Contributions to Embryology Carnegie Institution No.20 part 1

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Streeter GL. The histogenesis and growth of the otic capsule and its contained periotic tissue-spaces in the human embryo. (1918) Contrib. Embryol., Carnegie Inst. Wash. 8: 5-54.

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If like me you are interested in human development, then this historic embryology monograph by Dr. George L. Streeter has a wonderful detail and interpretation of the otic capsule formation as available (at that given point in time) using a significant resource of human material from the Carnegie Institute. Further historic material is available on the page Contributions to Embryology series. The magnifications stated in the figure and plate legends refer to the original published images, not those available online. My thanks to the Internet Archive for making the original scanned book available. Those interested in current hearing and skull development should read the online notes on Hearing and Balance Development and Skull Development

  Streeter Links: George Streeter | 1905 Cranial and Spinal Nerves | 1906 Membranous Labyrinth | 1908 Peripheral Nervous System 10mm Human | 1908 Cranial Nerves 10mm Human | 1912 Nervous System | 1917 Scala Tympani Scala Vestibuli and Perioticular Cistern | 1917 Ear Cartilaginous Capsule | 1918 Otic Capsule | 1919 Filum Terminale | 1920 Presomite Embryo | 1920 Human Embryo Growth | 1921 Brain Vascular | 1938 Early Primate Stages | 1941 Macaque embryo | 1945 Stage 13-14 | 1948 Stages 15-18 | 1949 Cartilage and Bone | 1951 Stages 19-23 | Contributions to Embryology | Historic Embryology Papers | Carnegie Stages | Category:George Streeter George Linius Streeter (1873-1948)

Modern Notes:

Hearing Links: Introduction | inner ear | middle ear | outer ear | balance | placode | hearing neural | Science Lecture | Lecture Movie | Medicine Lecture | Stage 22 | hearing abnormalities | hearing test | sensory | Student project

  Categories: Hearing | Outer Ear | Middle Ear | Inner Ear | Balance

Historic Embryology - Hearing 
Historic Embryology: 1880 Platypus cochlea | 1892 Vertebrate Ear | 1902 Development of Hearing | 1906 Membranous Labyrinth | 1910 Auditory Nerve | 1913 Tectorial Membrane | 1918 Human Embryo Otic Capsule | 1918 Cochlea | 1918 Grays Anatomy | 1922 Human Auricle | 1922 Otic Primordia | 1931 Internal Ear Scalae | 1932 Otic Capsule 1 | 1933 Otic Capsule 2 | 1936 Otic Capsule 3 | 1933 Endolymphatic Sac | 1934 Otic Vesicle | 1934 Membranous Labyrinth | 1934 External Ear | 1938 Stapes - 7 to 21 weeks | 1938 Stapes - Term to Adult | 1940 Stapes | 1942 Stapes - Embryo 6.7 to 50 mm | 1943 Stapes - Fetus 75 to 150 mm | 1946 Aquaductus cochleae and periotic (perilymphatic) duct | 1946 aquaeductus cochleae | 1948 Fissula ante fenestram | 1948 Stapes - Fetus 160 mm to term | 1959 Auditory Ossicles | 1963 Human Otocyst | Historic Disclaimer


The first monographic treatise on the anatomy and physiology of the ear was that published by Breschet in 1833. This work proved to be a very important one, both as regards the new observations contained in it and the constructive manner in which the facts then known were analyzed. The terminology of the ear region was a standardized and most of the names that were used or introduced by Breschet are in use in the literature of to-day. Before stating his views concerning the structures with which we are dealing, reference must be made to the work of some of his predecessors, and this will be given essentially as outlined by him.

The early anatomists were familiar with the bony labyrinth, but supposed that the spaces contained within it were filled with air. In 1707, however, Valsalva described the normal presence of a fluid in the labyrinth Avhich he compared to the fluid seen in serous cavities. The presence of this fluid was confirmed by Vieussens (1714). His observations were made chiefly on new-born infants, in which he studied the distribution of the labyrinthine fluid and found it present in the vestibule, the cochlea, and in the semicircular canals. The same fluid was also referred to by Cassebohm (1735) and Morgagni (1740). Uptothattinie no author had directed any particular attention to the labyrinthine fluid, nor had anyone attempted to assign any function to it other than that of moistening the auditory nerve. It was Cotugno (1768) who first endeavored to show that the labjTinthine fluid had some connection with the transmission of sound vibrations. He maintained that there was no air in the spaces of the labjTinth, but that it was everywhere filled with the fluid, which according to his description exudes from the ends of the capillary arteries that are distributed throughout the membrane that lines the cavity of the labyrinth. He described the fluid as being drained off by means of the two aqueducts. Because of the completeness of his description and the interest which he attracted toward the subject, the labyrinthine fluid was thereafter known for more than half of a century as Cotugno's fluid.

Any further advance regarding the nature of the labyrinthine fluid required a more detailed knowledge of the soft parts of the labyrinth. Nerve-like cords and semicircular tubes had been seen in the canals and membranous partitions and sacs had been seen in the vestibule, but it remained for Scarpa (1789) to establish the identity of the membranous labyrinth. He showed that in man and other mammals the semicircular tubes and the vestibular sacs are of the same nature and form one system, and that they are distinct from periosteum. He described how they open freely into each other and are filled with a limjiid fluid which distends them. This fluid was thereafter referred to as the fluid of Scarpa. Me recognized it in a general way as di.stinct from the lal)yrinthine fluid, in which all parts of the membranous labyrinth floated, but otherwise grants it no further attention.

The relations and significance of the fluid of Cotugno and the fluid of Scarpa were not completely recognized until the jniblication of the noteworthy monograph of Breschet (1833) of which we have spoken. He introduced the terms perilymph and endolymph, by which they have since been known. The existence of the cochlear duct was unknown to Breschet, but otherwise his description of the labyrinth spaces and their contained fluids is the foundation on which the more recent descriptions are principally based. He showed that the perilymph occupies all the space of the bony labyrinth that is not taken up by the semicircular tubes, the utricle (median sinus), and the saccule. It surrounds these everywhere and separates them from the bony walls of the labyrinth. The perilymph also, according to him, fills the spaces of the cochlea and circulates freely throughout the whole system. The scala tympani is connected at its apical extremity with the scala vestibuli by means of the opening to which he gave the name helicotrema. The scala vestibuli in turn opens freely into the vestibule, into which also the semicircular tubes open. He points out the fact, and discusses its relation to the mechanism of hearing, that any vibrations transmitted to the perilymph by the foot-plate of the stapes would be transmitted freely and evenly to the whole of the membranous labjTinth and to the lamina spiralis. He describes the perilymph as consisting of a thin, watery, saline fluid containing a small amount of albumin. He believed that it was secreted by the thin, delicate membrane lining the cavity of the labyrinth and that the materials were brought there by the small blood-vessels that supply this later. The aqueducts, according to him, are not for the transmission of perilymph, but only serve as passages for veins. He regards them of embryological significance; that they represent the remaining strands of connection with the dura mater, of which the inner ear is a part that has been separated off by the enveloping growth of bone. A description is given of the distribution of perilymph in different animals and it is pointed out that in some fish it communicates with the fluid surrounding the central nervous system and how in such cases the oily or gelatinous cerebro-spinal fluid actually serves as the perilymj^h. Entirely distinct from the perilymph is the endolymph, which is the fluid filling all parts of the membranous labyrinth.

Breschet describes the character of the endolymph in different animals. He shows that it always contains calcareous deposits, which he designates as otohths and otoconia, depending on whether they are in the form of lumps or dust. He shows that these are distributed at definite places, at the points of nerve-terminations, and suggests that they act as dampers that tend to check the prolonged vibration of the endolymph. In comparing the ear with the eye, he suggests that the perilymph bears the same relation to the organ of hearing that the aqueous humor bears to the organ of vision. The vitreous body he considers analogous to the endolymph.

Special emphasis has been given to the treatise of Breschet because it marks the beginning of the modern epoch in the anatomy of the ear. Previously the descriptions of this organ had been purely fragmentary. Breschet's monograph is both comprehensive and analytic. If his treatise is searched for defects that are revealed in the light of our present knowledge of the anatomy of the ear, one would name perhaps only two major ones. One of these concerns the inaccurate and meager nature of the embryological features as given by him, and the other concerns the membranous cochlea, the existence of which was entirely unknown at that time. It is interesting to note that these two defects prove to be related; that it was through embryological investigations that the membranous cochlea was eventually discovered.

At about the time of Breschet's treatise, Huschke (1831) made the discovery that the membranous labvrinth was originally a pit in the skin, a fundamental point that was confirmed later by other embryologists. He also found that in sheep and calf embryos the lamina spiralis is hollow, constituting a spiral tube that is closely attached to the bony walls of the cochlea. He evidently had before him the ductus cochlearis. He supposed, however, that the scalae in their formation flattened out this hollow tube, thereby converting it into the lamina spiralis, and thus he did not grasp the meaning of the structure and just missed being the discoverer of the membranous cochlea.

The significance of the spiral tube seen by Huschke in the embryo and its persistence as the ductus cochlearis in the adult remained to be pointed out by Reissner and Reichert in a series of communications published in the years 1851 to 1854, being based in large part on embryological studies of the chick and also of mammals. The first communication was the Dorpat dissertation of the former, completed in Reichert's laboratory. It contained an account of the ductus cochlearis (canalis cochlearis), which was shown to exist as a definite canal in the adult mammalian cochlea. It was pointed out that the membranous part of the lamina spiralis forms one-half of the wall of the canal and that the other half consists of a very thin and delicate membrane that is usually torn in the preparation of such a specimen. This portion has since been known as the membrane of Reissner.

Reissner and Reichert demonstrated the complete canal in infants at about term. In the embryo they found that the cochlear duct opens into the membranous vestibule, but whether or not it does this in the adult was not definitely determined. They give an account of the development of the ear in the chick, and they describe the formation of a labyrinthine groove in the skin and how this subsequently in vaginates to become the otic vesicle to which the acoustic nerve attaches itself later. They divide the early labyrinth into three chief ])arts: (1) recessus labyrinthi; (2) vestibule and its three canals; (3) cochlear duct. In a later paper Reissner (1854) refers to the formation of the scalse. He explains them as two accessory cavities that are formed because the cartilage recedes from the upper and lower surfaces of the cochlear duct. He denies the existence of any communication between the vestibular cistern (Hohle des Vorhofs) and the scala vestibuli both in the embryo and adult. His observations concerning the scalae have proved to be less important than those on the embryology of the otic vesicle and the discovery of the cochlear duct.

Kolliker (1854) had just at this time written the first edition of his "Gewebelehre" and had described at some length the finer structure of the cochlea, embodying his own and the important observations of Corti (1851). He makes mention of Reissner's dis.sertation, but there is no evidence that he appreciated at that time the significance of the cochlear duct. In a separate paper and in his text-book on human embryology, both of which appeared soon after this (Kolliker, 1801 a and b), he definitely establishes the existence of Reissner's membrane and that it forms the boundary of the cochlear canal. He confirmed the Reissner and Reichert embryological studies showing that the cochlear canal is originally an epithelial tube which is derived from the primitive ear-vesicle and hence from the ectoderm of the embryo. He designates the cochlear canal as the scala media, a term which persisted for many years, though its inapplicability was promptly pointed out by Reichert (18G4).

Kolliker is the first to describe in some detail the formation of the otic capsule and the perilymphatic spaces. The summary here given is taken from the second edition of his book (Kolhker, 1879), in which there is some amplification of the account given in the first edition. According to him, after the otic vesicle reaches a certain degree of development it is surrounded by a delicate connective-tissue membrane and there is an outer thicker and firmer mass which takes on the nature of cartilage, which in 19-mm. cow embryos forms an integral part of the wall of the skull. In human embryos 8 weeks old the labyrinth capsule consists of true cartilage and completely fuses with the base of the skull. He expresses the opinion that the cartilago petrosa is laid down exactly in the same way as the other parts of the lateral walls of the skull and that its special characteristics, subsequently assumed, are due to the presence of the special sense-organ.

In connection wath the origin of the cavities of the bony labyrinth, Kolliker draws attention to the problem of space formation in general and points out that the space in the otic capsule is of the tj^pe seen in the subarachnoid and other serous cavities. He describes how, along with the growth of the epithelial part of the labyrinth, there is also a rapid growth of its connective-tissue coverings, which soon attain considerable thickness. At the same time the periotic tissue becomes differentiated into three layers, of which the middle one soon becomes the thickest. This layer consists of a network of anastomosing connective-tissue cells (Gallertgewebe), whose rounded meshes are filled with fluid. From this there is gradually formed the cavity that surrounds the semicircular canals, the meshes becoming larger and finally coalescing. In the process of coalescence, parts of the cellular net are broken and other parts are pressed against the walls of the space, where, even in the adult, one can recognize remnants of the broken net. The same process takes place in the semicircular canals, the vestibule, and the cochlea. In the last-mentioned there are formed the two scalae, in which, in addition to the coalescence of the spaces of the network, there is also involved a disproportionate growth in respect to the cochlear duct and the surrounding cartilage, the latter retracting from the former by virtue of its rapid growth. Kolliker's conception of this process is purely mechanical, and it hypothesizes a protoplasmic network that is entirely passive. He did not conceive of an adaptive activity on the part of the protoplasm itself by virtue of which the characteristic changes in form are brought about, as is to be described in the present paper.

Among a series of miscellaneous notes concerning the development of the mammalian labyrinth appended at the end of KoUiker's chapter, there is a reference as to the relation of the growth of the cartilage to the growth of the contained spaces, which is particularly interesting, as it shows that he had in mind one aspect of the problem with which we are concerned. He notes there (p. 746) that at first the epithelial part is directh' surrounded by young cartilage, or better, a cartilage-like substance of which the greater part becomes subsequently converted into cartilage. In its further differentiation the tissue lying directly against the labyrinth becomes fibrous tissue and the tissue farther away becomes cartilage. Out of the uniform fibrous tissue there is further differentiated the inner perichondrium, the fiber wall of the labyrinth, and the cell tissue intervening between these. This intervening tissue untlergoes an independent growth characterized by a rich growth of blood-vessels. As a space, i. e., the cavity of the cartilago petrosa, it grows in correspondence to the growth of the epithelial labyrinth. As to the behavior of the cartilage during the growth Kolliker was undecided, giving the opinion, however, that it grew independently at the same time as the space, and was not simply mechanically stretched out.

The embryological studies of His began to appear at about the time of the publication of Kolliker's work on the ear, and one would rather expect that the attention of this keen observer would have been attracted to this subject. In his "Akademische Programme" of the year 1865 he outlines (His, 1903) the general problem of the formation of the various body-cavities and describes in detail the formation of the cavities of the middle germ-layer. He includes in this the arachnoid spaces and the cavities of the eye-ball, but he does not refer to the ear.

Inasmuch as the present paper is directly concerned only with the capsule of the ear and the contained periotic connective-tissue spaces, it will not be necessary to trace the further elaboration of a more precise knowledge of the structure of the membranous labyrinth which rapidly took place following the appearance of Koliker's text-bookand the introduction of the new histological and embryological methods which were devised in such abundance at about that time. A complete survey of such investigations is given in the monograph of Retzius (1884), to which the reader is referred. Our review here of the subsequent literature will be restricted to those publications having a special bearing on the periotic connective-tissue structures and the problem of their development.

The canalis reunions was discovered by Hensen (1863) as a communication existing between the ductus cochlearis and the sacculus. This established the relation of the cochlear duct as a definite part of the closed system of the membranous labyrinth, and its complete separation from the vestibular space. Using the terminology of Breschet, it thus constitutes an endolymphatic space, whereas the scala vestibuli and seal atympani are both perilymphatic spaces. Hensen also described the aquseductus cochleae. He regarded it as an invagination from the outer i)erichondrium into the cochlea by a i)rocess similar to the invagination of the aqueous humor of the eye. In the embryo it consists of a connective-tissue tube which is continuous with the primary periosteum. It si)lits into two limbs, the shorter one of which extends towards the round window and forms the lining of the proximal part of the scala tympani. The other limb of the membranous aqueduct extends towards the modiolus and unites with the dura mater of the acoustic nerve.

Hensen was followed by Odenius (1867) who gives a careful description of the position of the different parts of the membranous labyrinth and of the "perilymphatic" spaces surrounding them. He separates the perilymi)liatic space of the vestilnile into two divisions based on the attachment of the ut^ricle to the vestibular wall. The lower and chief division he names sinus perilymphaticus vestibuli. This communicates with the upper division, which surrounds the upper i)art of the utricle and extends along the semicircular canals. This part is narrower and is hardly more than a cleft situated between the membranous labyrinth and the bony wall and is traversed by many trabeculae.

A third author who could be put in this group is Boettcher (1869). He published two papers which bear upon the periotic spaces, but these are not available to the writer and resort has been had to the account of them given by Retzius (1884). He describes the formation of the scalae in sheep embryos. They make their first appearance in embryos 70 nmi. long, beginning in the first turn of the cochlea and gradually extending to the second and third. According to him there is a preliminary formation of mucus tissue in the region in which the scalie are to appear; this then undergoes a fatty degeneration, the result being the formation of the spaces. He warns against confusing this special " Schleimgewebe " with ordinary intracapsular connective tissue and opposes Hensen's theory of its invagination from the outer periosteum. According to him (Boettcher, 1872), it arises in loco out of the original cellular embryonal connective tissue.

Although it was recognized that there must be a provision in the human adult ear for the renewal and drainage of the intralabyrinthine fluid, yet there was no positive evidence of how this was accomplished until the introduction of injection methods. Schwalbe (1869) found that when Berlin blue is injected into the subdural space the injection mass passes through the internal auditor}' meatus into the space existing between the bony and membranous labyrinth. Since he could also trace the injection mass from the subdural spaces into the lymph vessels and glands, he therefore believed that the perilymph spaces represented true IjTnph spaces, for which the arachnoid spaces acted as the main drainage-channels.

In order to test out the communication reported by Schwalbe between the arachnoidal spaces and the perilymphatic space, a series of injections were made by Weber (1869), who found that the injected fluid accompanied the acoustic nerve as far as the lamina cribrosa, but did not go through this. It passed rapidly however, through the aquaeductus cochleae into the perilymphatic space of the cochlea. Later, this same investigator (Weber-Liel, 1879) invented the aspiration method by which the results were refined, and he was able to avoid the production of artificial paths which conmionly result where strong pressure is necessary for the injection and which apparently had vitiated Schwalbe's experiments. He proved clearly that the aquseductus cochleae was the primary path of communication between the perilymphatic and arachnoidal spaces, and that it consists of a free canal lined by an extension of dura mater connecting the scala tympani with the cranial cavity. He was not specific, however, as to whether the communication was with the subdural or subarachnoid space.

Key and Retzius (1875) in their extensive studies on the brain membranes, were able by injection methods to show that the spaces of the brain membranes stood in open communication with the perihonphatic space of the labyrinth, but, although they were able to trace the injection mass along the acoustic nerve, through the lamina cribrosa, and along the finer filaments of the nerve into the lamina spiralis, they were not sure of its communication there with the perilymphatic space. They showed, on the other hand, that the latter could not be injected through the aquiductus vestibuli and scemod convinced that the main communication was through the aquaductus cochleae as described by Weber, which view remains the [)revalent one to-day.

It may be added that Retzius (1884) subsequently made some further injection experiments in older fetuses and in the adult, which were published in his large monograph on the ear. He found (p. 330) that in this way the scala tympani communicates freely through the ductus perilymphaticus with the subarachnoid spaces, and not with the subdural space, which point had been left undecided by Weber. By injecting through either the round or oval window he was able to trace the escape of the fluid into the subarachnoid spaces, but never into the subdural space.

The comparative anatomists gave relatively little attention to the connective tissue spaces around the ear and there was consequently no great advance secured from this aspect of the problem. Hasse (1873, account taken from Retzius) investigated embryos of various mammals, but his results are confusing. Concerning the lymph tracts of the inner ear he showed that in man and other mammals, in embryonal and adult stages, there exists a channel to which he gave the name ductus perilymphaticus, which is the same channel through which the injectionists had forced their fluids into the scala tympani. Hasse described this as provided with a sac which connects on the one hand with the cavum subarachnoideale (the outer epicerebral space after sjjlitting the brain membranes into pia and arachnoid) and into a lymjih- vessel on the other. This drainage path of the "perilymph, " according to him, is not the only and in fact is not the chief drainage path; a similar path, consisting of a funnel-shaped sheath of arachnoid, projects into the internal auditory meatus accompanying the acoustic and facial nerves. In a later paper, Hasse (1881) reverses the importance of these two channels and describes the perilymph as flowing chiefly through the ductus perilymphaticus into the peripheral lymph system in the region of the jugular foramen, the same channel also draining the cerel)rospinal fluid of the subarachnoid cistern. There is also, according to him, some drainage from the subdural space through the internal auditory meatus.

Of more importance is the description of Retzius (1884). In his large monograph on the ear the gross and finer morphology of the periotic spaces and especially of the higher mammals, is described in greater detail and completeness than had previously been done. The comparative emliryology of the spaces is referred to by Balfour (1885). He speaks of lymphatic spaces (p. 522) as fonning in the rne.'^ol)last between the membranous labyrinth and the cartilage. These spaces are partially developed in Sauropsida, but become larger and more important in mammals, where they form the two scalse and the space surrounding the utricle and semicircular ducts. According to him the scahc begin to develop at the basal end of the cochlea, the cavity of each being gradually carried forward toward the apex of the cochlear canal by a " progressive absorption of the mesoblast. "

The descriptions of Retzius (1884) and of Kolliker (1861 b, 1884) and also the chapter in the sixth edition of the " Ciewebelehre, " rewritten by v. El)ner (1902), have had a prevailing influence on the present conception of the character and development of the tissues of the otic capsule. There should be mentioned with these also the work of Krause (1901), who studied the development of these struc- tures in a number of vertebrate forms. He finds that the first traces of the formation of a "perilymphatic space" occur some little time before the formation of the scala tympani, in the region lateral to the utricle and saccule. At this point the perilymphatic tissue becomes gradually fluidified and there arises between the lateral wall of the two sacs and the cartilaginous wall of the labj^rinth a large perilymphatic space " the cisterna perilymphatica " to which the foramen ovale serves as a direct approach. From this cistern the space-formation spreads into the cartilaginous semicircular canals and simultaneousl.v there begins the formation of the scalse, resulting finally in a cavity system that incloses the entire membranous labyrinth. Reference is made by him to the ductus perilymphaticus of Hasse, which connects this system with the subarachnoid spaces. This duct opens at one end in the vestibular part of the scala tympani and in the jugular fossa at the other. Concerning its development, nothing further was known.

In studying the development of the otic capsule, one is led into the general question of the growth of hyaline cartilage, for which there is an extensive literature and which is beyond the scope of the present paper. For general papers on this subject the reader is referred to those of Retterer (1900), Mall (1902), and Bardeen (1910). Other papers that may be mentioned as dealing particularly with the histogenesis of the skull are those of Solger (1889) and Filatoff (1906). An experimental study by Lewis (1907) should be referred to, in which it is shown that the production of the cartilaginous capsule is dependent upon the presence of the epithelial vesicle and that a transplanted otic plate becomes surrounded by cartilage derived from the tissue of the host.

The gross morphology of the cartilaginous capsule of the car has been described for several embryonic stages in connection with the cartilaginous skull as a whole, and mention may be made in this connection of the work of Gaupp (1906) and Terry (1917) on certain vertebrate forms and the papers of Levi (1900) and Macklin (1914) on the human embryo. The writer has also had the opportunity of studying a reconstruction of the otic capsule in a human embryo 21 mm. long made by Professor W. H. Lewis and one of a 43-mm. embryo made by Dr. Macklin, both of which were modeled in this laboratory and have not yet been published.

Carnegie Institution No.20 Otic Capsule: Introduction | Terminology | Historical | Material and Methods | Development of cartilaginous capsule of ear | Condensation of periotic mesenchyme | Differentiation of precartilage | Differentiation of cartilage | Growth and alteration of form of cartilaginous canals | Development of the periotic reticular connective tissue | Development of the perichondrium | Development of the periotic tissue-spaces | Development of the periotic cistern of the vestibule | Development of the periotic spaces of the semicircular ducts | Development of the scala tympani and scala vestibuli | Communication with subarachnoid spaces | Summary | Bibliography | Explanation of plates | List of Carnegie Monographs

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