Paper - The development of the ear-bones in the mouse

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Jenkinson JW. The development of the ear-bones in the mouse. (1911) J Anat Physiol. 45(4): 305–318. PMID 17232891

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This 1911 historic paper by Jenkinson describes early middle ear ossicle development in mouse.

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The Development of the Ear-bones in the Mouse

By J. W. JENKINSON, MA, DSc.


Lecturer on Embryology, University of Oxford, Fellow of Exeter College.


That in the whole of vertebrate morphology there has hardly been a question more vexed than that of the homologies of the auditory ossicles of the mammalia is notorious. For not only has the dispute been prolonged, but in it almost every possible interpretation has found its advocate.! The stapes has been regarded as a derivative of the auditory capsule, as the upper segment of the hyoid arch (hyo-mandibular) and as an independent element. The incus has been held to be the hyo-mandibular, by others a derivative of the mandibular arch. The malleus has usually been referred to the mandibular arch, though its hyoid origin has also been suggested. And all these various views have been differently combined by different morphologists. Thus—to take the more important—Huxley and Parker considered the stapes to be out out of the auditory capsule, the incus to be the homologue of the hyo-mandibular, and the malleus the representative of the quadrate. The older Continental view homologised the stapes with the hyo-mandibular, the incus with the quadrate, the malleus with the articular of lower types, while Gadow has attributed all three to the hyoïd arch.

  • 1 A full review of the subject will be found in the articles of Gaupp, quoted at the end of this paper.

But protracted though the controversy had been, it might well have been thought that with the work of Broman the issue was finally decided. For in Broman’s extremely thorough investigation of the development of these structures in the human embryo, use was made for the first time of reconstruction models, and in these models associated structures — notably the seventh nerve and chorda tympani—were inserted to aid in the accurate determination of the anatomical relations of the parts. Broman’s work corroborates the views held by Gegenbaur and other German writers.


The stapes is derived from the median dorsal portion of the hyoïd arch; it only comes secondarily into contact with the auditory capsule. The ventral and median portion of the hyoid arch becomes the stylo-hyal. It is at first connected with the stapes, but soon separates from it; later it becomes immediately connected to the auditory capsule. The incus and malleus are both derivatives of the mandibular arch.


Gaupp has pointed out that the relations of the seventh nerve and its mandibular branch, the chorda tympani, to these structures, as shown in Broman'’s figures, bear out the suggestion that the incus is the homologue of the quadrate, the malleus the homologue of the articulare, and the articulation between them the jaw-joint of the lower vertebrata.


But clear and convincing though Broman’s account is, it has not met with universal acceptation. : In two recent memoirs Fuchs has revived the old quarrel, and once more we have to inquire into the morphological value of these ossicles. In the rabbit, according to Fuchs, the stapes is derived from the auditory capsule, its original blastema being perfectly continuous with that which surrounds the auditory vesicle. Further, the blastema of the stapes, in the earliest stage seen by Fuchs, lies median to the first gill-slit, that is, to its endodermal portion or pharyngeal evagination, The stapes is not originally connected with the blastema of the hyoid, as the latter only reaches dorsally as far as the point at which the chorda tympani leaves the seventh nerve. The connection later found between the two—ligamentum hyo-stapediale—is purely secondary.


To the malleus and incus Fuchs concedes a derivation from the mandibular arch, but refuses to allow the homology between them on the one hand and the articular and quadrate on the other. The malleus and incus, he maintains, spring from a blastema which lies in the dorsal portion of the mandibular arch, but is quite independent of the blastema for Meckel’s cartilage, though, admittedly, lying in the same straight line with it. In support of this interpretation, Fuchs urges that chondrification begins at the upper end of Meckel’s cartilage—at a point where later the jaw-joint will be developed, and just where the nervus auriculo-temporalis comes off the fifth nerve to pass outwards behind the condyle of the mandible. This chondrification begins before any cartilage is formed in the malleus or incus, and extends distally along Meckel's cartilage. In the malleus and incus cartilage is formed independently, and the connection, by means of the processus gracilis, between the malleus and Meckel’s cartilage is a later and secondary development. On the other hand, Meckel's cartilage is stated to be proximally continuous with a more laterally placed chondro-blastema in which the jaw articulation is developed. The proximal half of this articulation becomes later continuous with the squamosal, the distal with the dentary. In these two elements, Fuchs finds the homologues of the quadrate and articular.


I have not myself examined the rabbit, but I have in my possession a number of preparations and reconstruction models of a not very distantly related mammal—the mouse—and, as these do not bear out Fuchs’ statements, I must beg leave to describe my observations as briefly as possible.


Mÿ material includes eight stages :—i. comprises embryos of 5.6 mm.


Fig. A.—Stage i. Model of left half of pharynx, seen from the inside,

M., mouth cavity; 1, 2, 8, and 4, first, second, third, and fourth gill- evaginations ; Hy.Bl., blastema of hyoid arch; A.C., auditory capsule ; VIL., seventh nerve ; St.A., stapedial arte EY.

I have not the dimensions of ïi., iii. and iv., but stage v. is 8 mm. long, and stage vi. 11 mm. Stage viii. is nearly full-time.

I. Stage i. (figs. À, and 1 a and b). Fig. À is a reconstruction of the left side of the pharynx and includes the blastema of the hyoïd (Hy. BL), the seventh nerve (vii.), and the auditory capsule (A.C.).

The four gill-slits—pharyngeal outgrowths—are seen, of which the first or hyo-mandibular slit is by far the largest. Behind this lies a mass of tissue, the blastema of the hyoid, the internal portion of which is traversed by an artery derived (fig. 1 b) from the aorta, the stapedial artery. This is therefore the first rudiment of the stapes, and it is perfectly continuous with the rest of the blastema on the outside. Model and sections alike show that the hyoid blastema lies behind the gill-evagination, just where this meets the ectodermal gill-cleft. The seventh nerve passes through the blastema and eventually emerges on its posterior side. There


Text, a. More anterior and dorsal section. b. More posterior and ventral section, A.V., auditory vesicle; A.C., auditory capsule; Ve. St.A., stapedial artery. Other letters as before. vena lateralis capitis ; VII.,seventh nerve ; Hy. B1.! blastema of the hyoïd arch; Ao., aorta ; 1, first

gill-evagination; 1. ext., first external gill'cleft.

Fic. 1.—Stage i.


Fic. 2.—Stage ii.

St., stapes ; Md.BI1., blastema of mandibular arch; V., fifth nerve. Other letters as before.

is another blastema which is quite independent of the stapes. This has the form of a shallow saucer embracing the outer side of the auditory vesicle (fig. 1 a). Its concave side is seen in the model. This is the beginning of the auditory capsule.

IT. In the second stage (fig. 2) the stapes rudiment is better defined. It is still perfectly distinct from the auditory capsule. It may now be described The Development of the Ear-Bones in the Mouse 309

as lying median to the dorsal portion of the first gill-evagination. This dorsal portion is being detached from the ectoderm, reduced in size, and laterally flattened.

AC vil


a. Dorsal section. b. More ventral section.


c. Still more ventral section.

Ch., chorda tympani. Other letters as before. Hy., anterior cornu of the hyoïd (stylo-hyal).

Fic. 8.— Stage iii.

IT. (Fig. 3, a, b, and c). In the third stage the gill-slit is much reduced dorsally (fig. 3, « and b); ventrally it is still large (fig. 3 c).

The stapes is still perfectly separate from the auditory capsule, but remains at present connected to the hyoïd (lateral hyoid, stylo-hyal) by a rather narrow bridge of tissue (fig. 3 b).


b. The same, from the inside, and from in front,

Ma.h., head of malleus; Ma.m., manubrium ; Pr.g., processus gracilis; Hy., hyoid (stylo-hyal); In., incus ; 1, first gill-evagination. Other letters as before.

Fia. B.—Stage iv. The Development of the Ear-Bones in the Mouse ST

In the mandibular arch there is a blastema, and, as the dorsal portion of the gill-slit becomes reduced, the inner dorsal part of this blastema grows inwards and backwards towards the stapes (fig. 3 a). This will be the


b. More ventral section.

a. Dorsal section. In., incus; Ma., malleus.


Still more ventral section. The stapes is here still connected to the hyoid. Other letters as above,

Fic. 4.1—Stage iv.

C.

incus. It is therefore by the reduction of the dorsal part of the first gillslit that the mandibular arch (ineus) is enabled to approach and come into contact with the hyoid arch (stapes).

1 In these figures the left side is lateral, the right side median. In all the previous figures of sections and in all that follow the reverse is the case,

The chorda tympani is seen (fig. 3 c) passing on to the median side of the mandibular blastema.

- IV. (Fig. B, a and b, fig. 4, a, b, and c). As may be gathered from the model and the section (fig. 4 c), the stapes is almost, but not yet quite, detached from the upper end of the hyoid. On the other hand, it has become embedded by its upper border in the auditory capsule. This is not


Fi. C.—Stage v.

Model (left side), from the inside.

Pr.l.i., processus longus incudis. The processus brevis is hidden behind (on the outside of) the . vena lateralis capitis (Ve.). Other letters as above.

shown in the model, but may be seen in fig. 4 a. The stapedial artery is represented in this model and appears, of course, in the sections.

In the mandibular arch there is a trace (fig. 4 b) of the articulation between incus and malleus.

The first gill-cleft (1) has been modelled in. It will be seen (fig. B b) that the dorsal portion of the cleft is reduced and_very much compressed. It lies obliquely. The stapes, which originally lay wholly behind the slit (Stage i.), is now behind and internal to it, while the incus and malleus are now in front of and external to it. It is over the top of the gill-slit that the incus approaches the stapes. The Development of the Ear-Bones in the Mouse 313

V. Fig. C and fig. 5. The stapes is now completely separated from the hyoïid, while the latter is becoming attached to the secondary tissue which is added on to the original auditory capsule external to the seventh nerve and the vena lateralis capitis (fig. 5).

The articulation between incus and malleus is apparent.

By means of its backwardly and inwardly directed processus longus the former is practically in contact with the stapes. The dorsally directed processus brevis lies external to the vena lateralis. In the head of the malleus chondrification is now beginning, in the processus gracilis it is more advanced. The manubrium is very well developed and pushes in the outer wall of the gill-slit.


Fig. 5. —Stage v. Ma., head of the malleus ; Pr.g., processus gracilis. Other letters as above.


In the last model (Fig. D, stage viii.) the ossicles have practically attained their final form. The sections (figs. 6, 7, and 8) illustrate the development of the fenestra ovalis during the last three stages.


The stapes becomes, as we have seen, embedded in the waïl of the auditory capsule. The tissue of the latter, which is immediately internal to and around the stapes, becomes converted, not into cartilage, but into fibrous tissue.


The layer immediately internal to the stapes and separating it, therefore, from the perilymphatic space, becomes thinner and thinner, the cells and nuclei flatter and Hatter. It is the lamina stapedialis. It is the only contribution which the auditory capsule maäkes to the stapes. The cells which surround the stapes, on the other hand, become radially elongated (radially with regard to the centre of the fenestra ovalis) and form the ligamentum annulare suspending the stapes in the fenestra. The fenestra, of course, is bounded by the surrounding cartilage. This account is in accord with the statements of Gradenigo (man, cat) and Dreyfuss (man, rabbit, guinea-pig, sheep).



Fic. D.—Stage viii. Model (left side) seen from the inside. (The photographer has accidentally tilted the -. manubrium too far back.)

Pr.b.i., processus brevis incudis. It lies in a concavity of the auditory capsule, part of which has been modelled in (A.C.).


Fic. 6. —Stage vi. Fi. 7.—Stage vii. Showing relations of stapes, stapedial artery and Showing formation of lamina stapedialis (L.st.) fenestra o7ahs(F.o.). Letters as before. and ligamentum annulare (L.a.).



Fic. 8.—Stage viii.

Further differentiation of fenestra ovalis and associated structures.

According to this account, therefore, the stapes is derived from the dorsal median portion of the hyoid arch. This portion of the hyoiïd blastema becomes perforated, in the earliest stage, by the stapedial artery. It then assumes a rounded form and is constricted off from the rest of the hyoid blastema. This ventral residue becomes the stylo-hyal or anterior cornu of the hyoid. Originally perfectly distinct from the auditory capsule, the stapes becomes secondarily embedded in it. The blastema of the latter internal to the stapes becomes differentiated into the lamina stapedialis, a thin membrane separating the stapes from the perilymph. This is, therefore, the only part of the stapes derived from the auditory capsule. The blastema immediately surrounding the stapes becomes the fibrous ligamentum annulare, supporting the stapes in the fenestra ovalis.


The incus and malleus are formed in the upper part of the blastema of the mandibular arch.


This dorsal portion of the blastema is in the same straight line as, and perfectly continuous with the ventral portion which gives rise to Meckel’s cartilage. The connection between the two by the processus gracilis is therefore primary and not secondary. It is, at the same time, perfectly true that chondrification begins at the level of the future jaw articulation, and proceeds distally. Later it proceeds proximally from this point into the processus gracilis and malleus. The connection of the incus with the stapes is effected by the backward and inward growth of the former over the first gill-slit, when the dorsal portion of the slit has disappeared.

The foregoing description is not in accord with Fuchs’ observations on the rabbit.

The stapes, according to the interpretation of this author, is a part of the auditory capsule, who finds that in his earliest stage (1) the blastema for the stapes is perfectly continuous with that for the auditory capsule, and (2) the stapes lies median to the dorsal recess of the first gill-cleft.


I cannot help believing that this is erroneous, and that Fuchs has not seen the earliest possible stage. The point at which he starts is equivalent to my stage iv., and in the mouse, at any rate, it is possible to find earlier conditions (stages i.-iii.) in which the stapes blastema is perfectly distinct from the auditorÿy capsule. On the other hand, in these stages it is certainly united to the tissue of the future hyoid, and the union still remains in stage iv. It is true that in this and the previous stage the connection between the two is by a narrow band of tissue only (figs. 4c and 8 b); but in the first stage there is but one mass of blastema in the second arch, and the dorsal median portion of this is perforated by the stapedial artery. I cannot, therefore, agree with Fuchs that the connection between stapes and hyoïd is purely secondary.


And, lastlÿ, the assertion that the stapes lies median to the gill-cleft is, though true, irrelevant. This position is secondary and due apparently to the rotation of the ear-bones, the stapes moving forwards and so coming to lie internal, the incus-malleus backwards and so coming to lie external to the slit. The slit in this (dorsal) region becomes reduced and compressed (fig. B b). The original position (fig. A) of the stapes is, with the rest of the hyoid arch, undoubtedly behind the hyo-mandibular cleft.


Fuchs’ account of the origin of the incus and malleus is not so easy to criticise. Though derivatives of the mandibular arch, he denies to them any original continuity with Meckel’s cartilage.


It is true, as he maintains, that chondrification begins in Meckel’s cartilage at a point some way in front of (distal to) the incus and malleus, at the level of the future jaw-joint, and proceeds from that point in a distal direction. It is also true that cartilage appears later and independently in the incus and malleus. But though at an earlier stage the blastema for Meckel’s cartilage is for this reason darker—the cells and nuclei being more closely packed—than in the incus malleus region, the two are in the same straight line and appear absolutely continuous, while at a still earlier date there appears to be a single blastema, continuous throughout, and with the cells equally densely packed in its proximal and distal regions.


Fuchs hypothesis encounters the further difficulty of making the blastema of Meckel's cartilage bend sharply to the outside and pass into the tissue of the future jaw-joint, while later on the same cartilage has to dissociate itself from the jaw-joint and become continuous, by the processus gracilis, with the malleus, the jaw-joint then uniting with the squamosal above and the dentary below.


The homology of the incus and malleus with the quadrate and articulare respectively does not, however, rest upon the embryological evidence alone. This evidence, we may take it, certainly proves the mandibular origin of these two ossicles. Whether, further, the articulation between them is the homologue of the jaw-joint of the lower forms must be left for the comparative anatomist to determine, though it may be pointed out that, as Gaupp has insisted, the course of the chorda tympani—external to the hyoïid, external to the gill-evagination, internal to the incus and malleus and so, alongside the processus gracilis, on to the fifth nerve—is in mammalian embryos extraordinarily similar to its relations to the hyoid, tympanic cavity, quadrate and articular in the lower types, especially in so primitive a form as Sphenodon.


Literature

E. Gawpr, ‘‘Ontogenese und Phylogenese des schallleitenden Apparates bei den Wirbeltieren,” Merkel und Bonnets Ergebnisse der Anatomie und Entwickelungsgeschichte, viii., 1899.

E. Gawuprp, ‘Die Entwickelung des Kopfskelettes,” in O. Hertwig's Handbuch der Entwickelungslehre der Wirbeltiere, Jena, 1906. 318 The Development of the Ear-Bones in the Mouse

I. BRoMAN, ‘Die Entwickelungsgeschichte der Gehôrknüchelchen beim Meuschen,” Anat. Hefte (1t° Abt.), xi., 1899.

. H. Fucus, ‘ Bemerkungen über die Herkunft und Entwickelung der Gehôrknôüchelchen bei Kaninchen-Embryonen,” Arch. f. Anat. und Phys. (Anat. Abt.), Suppl., 1905.

H. Fucus, “ Nachtrag zu meiner Arbeit: Bemerkungen über die Herkunft, etc.’ ibidem, 1906. G. GRADENIGO, ‘Die embryonale Anlage des Mittelohres,” Mitt. Embr. Inst.

Wien, i., 1880.

R. Drevruss, “ Beiträge sur Entwickelungsgeschichte des Mittelohres und des Trommelfells,” Morph. Arb., ïi., 1893. |


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