Talk:Paper - The early embryology of the auditory ossicles in man
The Early Embryology Of The Auditory Ossicles In Man: Illustrated In Atlas Series
Jerome R. Hanson, M.S., Barry J. Anson, Ph.D. (Med. Sc.) and Theodore H. Bast, Ph.D.*
INTECEDENT phases of an_ otological investigation, carried out at Northwestern University and the University of Wisconsin de: ut with developmental stages in which the otic capsule,
the auditory ossicles and the related branchial arches were well formed in cartilage.t As a recent supplement
to these more general discussions, three articles have offered detailed information on the morphogenesis of the otic capsule, the stapes and the incus (with atlas arrangement of figures). A fourth article, comparably concerned with the malleus, is in preparation.
It now remains to report upon the de 'From the Department of Anatomy of the University of Wisconsin and the Department of Anatomy of Northwestern University Medical School (Contribution No. 640 from the latter department).
A study carried out with the continuing support of the Central Pica of Research of the American Otological Society and of the National Institutes of Health of the United States Publie Health Service (Grant No. B. 2237). The cost of engravings was met by the use of the NIH grant.
Based upon a thesis presented by Jerome R. Hanson for the degree of Master of Science at the U niversity of Wisconsin; enlarged as a collaborative investigation, during his service as Project-Assistant on the above-named grant.
The drawings were executed by Miss Jean McConnell. The photomicrographs were taken by Mr. Homer Montague, labelled by Miss Rosamond Howland.
The authors are indebted to Dr, Shafik F. Richany who provided valuable assistance during the initial phase of the investigation.
Received for publication September 18, 1959.
- The illustrations were prepared from the following
series in the G. L. Streeter ( ‘ollection, Carnegie Laboratory, Baltimore, Kr sries 617; Figs. 3 and 4, 6517;
59;
Fig. 5, Fig. 6, 6524; Figs. 8 and 9, 4430: and from the
D; H. Bast Collection, University of Wisconsin, Fig. 7,
series 180; ligs. 10 and 11, 10; Fig. 12, 174; Figs. 13, 14,
15 and e ir fig. 17, 168; Fig. 18 : Fig. 19. B 124;
Vig. 20a, 13; Fig. 20b, 294; ( : Fig. 20d, 98.
Magnific an reconstructions: Fig. Dex 32; Figs.
3, 5, 6 and 7 X 20; Figs. 8 and 10, X 18; Fig. 12, X 16,
Fi ‘ig. 13, X 2
Magnifie =m fie ea eens Vig. 2, X 120; Figs. 4 and 9, X 69; Figs. 14 and 15, X 81; Fig. 16. X 25; Fig. 17x 5, i gs. is a 19, X 33; Figs. 20a and 20 b, X 20; Fig. 20e, X 13 20d, X 12.
‘Deceased January 1
‘Pertinent articles already have been cited in an earlier issue of this journal (vol. 32, 1958, pp. 157-172).
‘Anson, B. J. and Bast, T. H.: Development of the Otic Capsule o. the Human Ear. Quart. Bull. Northwestern University Medical School, 32:157-172, 1958.
Anson, B. J. and Bast, T. H.: Development of the Stapes of the Human Ear. Quart. Bull. Northwestern University Medical School, 33: 44-59, 1959.
Anson, B. J. and Bast, T.H.: Development of the Tneus of the Human Bar. Quart. Bull. Northwestern University medical School, 33: 110-119, 1959.
358
Developmental steps, taken before the stage of 28-mm., in which localized portions of the mesenchyma in the branchial region suddenly become distinguishable from the tissues of which they are primordially a part and, at the same time, assume an appearance and a position predictive of their adult form and topography.
In order to determine accurately the origin of the ossicles it is necessary to examine them prior to the aforementioned stage, beginning with specimens in which the future ossicles and the related branchial arches have not reached pre‘artilaginous constituency. In the past, investigators attempted to explain the origin of the ossicles without benefit of surly embryos. In such studies, limited as they were to the use of embryos in which the branchial arches and_ their derivatives were already composed of ‘artilage, conjecture inescapably took the place of fact in the attempt to account for the genesis of the auditory ossicles in man.®
Microscopic sections used alone are of limited value in following the rapidly changing architecture of the branchial arches, but reconstructions provide the needed aid in determining what contribution the mesenchymal condensations give the developing structures.’ The following discussion will be based chiefly upon the use of such ‘‘models.”’
In the fifth week of fetal life the stapes is not yet a definitive portion of a
‘Reviews of the literature on ossicular development have been presented by Fraser (1882), Gradenigo (1887), Dreyfuss (1893), Gaupp (1899), Broman (1899), Kingsley (1900), Fuehs (1905), Reagan (1917), van der Klaauw (1924), and Cauldwell and Anson (1942). Translations of the German literature prepared by Mrs. Eycke Strickland have been used as guidance in this present study. A complete presentation of the literature on early embryology of the ossicles by Mrs. Strickland and the present authors 1s Jn preparation,
‘As the authors have commented before, only by the use of reconstructions ean the continuity of fluctuating tissues and interrelationships of shifting structures be
established to the conviction of the writer and be pictured to the satisfaction of the reader. HANSON ET AL.—AUDITORY OSSICLES
blastemal lobe which is situated at the proximal extremity of the hyoid (Reichert’s) bar (fig. 1). This lobe is grooved by the facial nerve, which serves to divide it into a stapedial primordium and the laterohyale, both of which temporarily retain hyoid continuity (fig. 2). In the 9.6-mm. stage the division is more definitely marked. The portion which connects the above-mentioned structures is called the interhyale (fig. 3); it will give rise to the stapedial tendon.
In the earliest stages the two visceral bars are broadly connected by an interbranchial bridge of mesenchyme (figs. 1 and 3), the greater part of which is in the territory of the second arch as indicated by its relationship to the pharyngeal groove (figs. 3 and 4). This blastemal mass is located between, and continuous with, the middle segment of the hyoid bar and the proximal portion of the mandibular (Meckel’s) bar. This circumstance indicates that the manubrium of the malleus and long crus of the incusare mainly of second arch origin.
In the 8-mm. specimen, which is more advanced in ossicular development than the 9.6-mm. stage, the interbranchial bridge is separating from the hyoid bar along a suleus which transmits the chorda tympani (fig. 5). Separation is complete in the 11.7-mm. stage, at which time a secondary connection between the arches is formed as the incus, now of distinguishable outline, comes to approximate the stapes (fig. 6).
During the fifth week the stapedial artery attains 2 central position in the blastemal lobe, thereby seeming to aid in the conversion of the rounded mass into a ring-like structure with an obturator foramen (figs. 5 to 9). Oceasionally a ring fails to form, and an anomalous stapes is the result; the horseshoe-shaped stapes in a [4-mm. embryo is an example of this defect (fig. 7).
The malleus and in¢us in the 15.5-mm. embryo, although still precartilaginous, become demarcated as the manubrium and long crus begin to assume characteristic form and as a groove appears between the head of the malleus and body of the incus (fig. 8). At this stage the ring-shaped stapes impinges upon the otic capsule. The laterohyale and short crus of the incus end in loose adventitia (fig. 9). In the 17-mm. embryo, both the incus and malleus are clearly identifiable as chondrified structures. The malleus temporarily remains in continuity with the mandibular (Meckel’s) bar (fig. 10).
The interhyale passes from the junction of the stapes and incus to the hyoid bar (fig. 11) where the latter makes an acute angle to become the laterohyale (in contact with capsular tissue). The primordium of the stapedial muscle is identifiable in the 21-mm. stage (fig. 12) as an outgrowth from the interhyale, located posterior to the angle of Reichert’s cartilage and medial to the facial nerve (figs. 13 and 14). The tendon of the stapedial muscle is derived from the interhyale in the portion between the developing stapes and Reichert’s bar (figs. 15 and 16). The stapedial ring now fuses with the otic capsule, the conjoined tissue thus becoming the lamina stapedialis. The periphery of the lamina, through differentiation of its tissue. will become the annular ligament. The zone of change is the site of the future vestibular fenestra (fig. 15).
Continuity between the interhyale (seemingly the primordium of the stapedial muscle as well as the tendon) and the laterohyale is lost in the 40-mm fetus; at this stage the constituent cells begin to assume the appearance of muscle (fig. 17).
As the muscle develops and the incudostapedial joint is formed, the tendon usually gains an attachment to the neck stapes. However, the frequent partial insertion of the stapedial tendon into the incus (figs. 18 and 19) supports the belief that the long crus of the incus, as well as the stapes, is a derivative of the second arch.
Both of the cartilaginous arches contribute not only to the substance of the auditory ossicles, but also to that of related structures in the head and neck.
‘Bast. T. H., Anson, B. J. and Riechany, 8. Development of the Second Branchial Arch Cartilage), Facial Canal
Man. Qi Bull. Northwestern School, 30 5-249, 1956.
Richany, F.. Bast, T. H. and Auson, B. J.: The Development of the First Branchial Are in Man and the Fate of Meckel's Cartilage. Quart. Bull. Northwestern University Medica! Sehool, 30: 331-355, 1956.
F.: The Reichert's and Associated Structures in Medieai
While the malleus is undergoing ossification, the zone of continuity with
Meckel’s cartilage narrows rapidly (fig.
20a). This alteration in form is due to
a retrograde change in the cartilage which
precedes differentiation of the tissue
into that of the future anterior ligament
of the malleus. As soon as bone is
formed in the head and neok of the
malleus the anterior process (an osseous
rod before bone-formation begins in the
ossicle itself) fuses with the malleus
(fig. 20b). Distally the cartilage will be
absorbed in the mandible.
Reichert’s cartilage passes through an even more dramatic series of changes in attaining adulthood. At its proximal extremity, that part of the cartilage which is derived from the laterohyale of the
early embryo forms a transitory lateral boundary for the developing facial canal (fig. 20c). By the 215-mm. stage, however, membrane bone is developing internal to the cartilage—thus intervening between cartilage and nerve (and stapedial muscle, derived from the interhyale). Concurrently, the otic capsule is ossifying. In early infancy, Reichert’s ‘artilage is merely a remnant within new bone, and the facial canal has acquired new and permanent walls (fig. 20d). Distally the tissue of the original arch is converted into the styloid process of the temporal bone, the stylohyoid ligament and the lesser cornu of the hyoid bone.
The 2llustrations appear on the succeeding pages. HANSON ET AL.—AUDITORY OSSICLES 361
Embryo, 7mm.
ae REICHERT’S CARTILAGE Stapedial a yp». (branchial arch I)»
_-- Stapedial
blastema
Laterohyale
(Broman )
MECKEL’S CARTILAGE setae (branchial arch I)
Stapedial a’ Facial nerve laterohyale
‘Chorda tympani
Posteroinferior view
SUPERIOR
\.. Facial nerve
=, ~Blastemal mass for stapes
POSTERIOR
C. Laterohyale~*
ANTERIOR 4 Chorda tympani INFERIOR
Fig. 1. In the embryo of 41/2 weeks (7mm.) the precursor tissue for the auditory ossicles is @ common blastemal mass which is distinguishable from the surrounding mesenchyma only because of the greater concentration of its constituent cells (compare fig. 2).
A lobe-like portion of this mass is located at the cranial end of the second visceral bar (precursor of Reichert’s cartilage), where it is grooved by the facial nerve. Part of this mass is the primordium of the stapes. However, it is still separate from the aggregation of cells which will become the otic capsule (the latter not included in the reconstruction). The stapedial artery extends from its sourcevessel to encroach upon the interiomedial aspect of the blastema (fig. 1a); the chorda tympani branches from the facial nerve to pass medial to the first visceral bar, the forerunner of Meckel’s cartilage (fig. 1b).
A mesenchymal bridge of cells between the first and second visceral bars extends from the proxi mal end of the mandibular bar (at I in fig. 1c) to a point on the hyoid bar (at IT) just distal to the blastemal lobe of the stapes (fig. 1c). The primordia of the malleus and incus are not yet distinct structures within this condensation of cells which will soon give rise to them. 362 QUARTERLY BULLETIN, N.U.MLS.
7mm. Glossopharyngeal
Stapedial artery
(origin)
Ag: — Laterohyale
4 Pharyngeal
> groove
f rea 4 imae 3 4 a ag .
avs : PP MeO a Gi
aso, PaO TT ae
Fig. 2. As is clearly demonstrated in sections, the common blastemal lobe is situated dorsal to the first pharyngeal groove, where it is indented by the facial nerve on its dorsolateral aspect. It is through the presence of the sulcus produced by the nerve that the following forecast may be made: the medial and larger part of the lobe will give rise to the stapes; the part lateral to the nerve will become the laterohyale; the interconnecting portion, which is still very broad, will become the interhyale. The narrowing of the interhyale and subsequent separation of the stapedial portion from the laterohyale is seemingly influenced by the pressure of the facial nerve, as this mass increases at a more rapid rate than does the nerve itself.
The presence of the stapedial artery identifies part of the general blastema as the ‘‘stapes’’; it is still solid, not having yet acquired the form of an annulet. The future position of the artery in the center of the mass appears to be due to a folding around the artery as the blastema enlarges. The process seems to be one of envelopment of the artery by growth of the mass rather than one of perforation through elongation of the vessel,
Al this stage the blastema may be said, for the first time, to possess a distinguishable boundary. In the 6Yo-mm. stage the tissue in the corresponding branchial area is a simple, diffuse mesenchyme. HANSON ET AL.—AUDITORY OSSICLES 363
Embryo, 9.6mm.
a.
REICHERT’S CARTILAGE (IL)
4 /
levee as / SMa Blastemal masses:
Interhyale-* stapes
.-Malleus , incus - .~S_Facial nerve Anterosuperior view | wot
MECKEL’S CARTILAGE oy .
Trigeminal nerve
-Laterohyale
.~Incus > malleus
I Spacek Posteroinferior View
SUPERIOR
Blastema of stapes-_" 7
C. ANTERIOR
I Blastema of malleus, incus
| Lateral view INFERIOR
Fig. 3. In the embryo of 512 weeks (9.6 mm.) the branchial structures have increased greatly size through hyperplasia of the mesenchymal cells and the outlines of the ossicular primordia have become more clearly defined.
The second visceral bar projects farther toward the otic labyrinth than the first and has at its proximal extremity the blastemal lobe with the primordium of the stapes. The facial nerve has grooved the lobe more deeply, the sulcus serving to mark off more distinctly the stapedial from the laterohyale portion. The primordium of the stapes is still separated from the otic capsule (not shown) by a zone of cells which is less dense than the mesenchyme of either the stapes or the capsule. The general location of the stapes (lateral to the otic capsule and medial to the facial nerve) is one which persists throughout fetal life and into adulthood.
Although a stapedial artery is not yet centrally located within the blastema, an artery is found (not shown in the reconstruction) at the periphery of the lobe as it was in the 7-mm. stage.
The malleus and incus are not yet differentiated from the interbranchial bridge of mesenchyme which now broadly connects the two visceral bars across the first pharyngeal groove (fig. de at arrow). Since the groove is the boundary externally between the arches (I and II), double origin of the two ossicles is thereby indicated.
The chorda tympani, branching from the facial nerve, passes from the hyoid arch (IT), inferior to the blastemal mass, into the mandibular arch (1). It appears as if the nerve were playing an important role in the separation of the blastema from the second visceral har.
Blastema of laterohyale
POSTERIOR b~Facial nerve
/ Nf 364 QUARTERLY BULLETIN, N.U.MLS.
Second visceral ar
Pharyngeal
cavity _ _ ee
nerve
Fig. 4. The first pharyngeal groove makes a deep impression on the lateral aspect of the blastemal mass which is established as the primary connection between the first and second visceral arches. The first visceral bar is located closer to the groove than is the second bar, meaning that the major portion. of the cellular mass belongs to the second arch.
Although no longitudinal grooves or differences in cellular density exist to distinguish the primordium of the malleus from that of the incus, the relationships to adjacent structures and the course of the chorda tympani (about to branch from the facial nerve) are indications that this mesenchymal mass is the source-tissue of both of these ossicles.
As seen in neighboring sections, the chorda tympani, after branching from the facial nerve, passes medial to the pharyngeal groove and into the first visceral arch, where it joins the mandibular branch of the trigeminal nerve. The pathway of this nerve from the lateral to the medial side of the blastema serves to separate the primordium for the malleus and incus from the second visceral bar. A large portion of this mass is located on the second arch side of the pharyngeal groove, suggesting that most of the primordial tissue which will develop into the manubrium of the malleus and long crus of the incus comes from mesenchymal cells which are of second arch origin. This contradicts the usual belief that the malleus and incus are derived entirely from the first arch. HANSON ET AL.—AUDITORY OSSICLES Embryo, 8mm. a. REICHERT’S CARTILAGE
Hyoid arch
‘ \
Facial nerve
LL
Interhyale
~Blastema of malleus and incus
MECKEL’S }
‘ é tympani, . he Mandibulay! A — Anterosuperior view nerve, A E rideminal nerve
_Hyoid , b.
Facial nerve-. vayeh
- A
Chorda tympani
A Ld,
Blastema for 2malleus and incus
Tyigemunal--- C.
nerve
SUPERIOR | Trigeminal
Mandibular nerve, TLSYVS
Lateral view
() POSTERIOR
ANTERIOR Malleus and incusy” “Interhyale
Ni
Laterohyale
4 Chorda .” Facial nerve
tympani Hyoid INFERIOR
Fig. 5. In the 8-mm. (5-week) embryo branchial development is advanced over that of the‘9.6-mm. stage in respect to the following: deeper entry of the stapedial artery into the stapedial anlage; further separation of the laterohyale from the stapes by the facial nerve; almost com plete rupture of continuity of the interbranchial bridge adjacent to the second visceral bar (through the influence of the chorda tympani). Whether the 8-mm. specimen is advanced, or the 9.6-mm. specimen is retarded in development, cannot, of course, be determined.
365 366 QUARTERLY BULLETIN, N.U.MLS.
Embryo, 11.7 mm.
a. REICHERT’S CARTILAGE « a. Interhyale > “Weta Sg = 2: Wx, Laterohyale - Stapes -Incus Malleus
——_— e a
Anteroguperior vi¢w
MECKEL’S CARTILAGE
Blastema of hyoid cartilage \ x /
/
erg Malleus
Posteroinferioy view .
Incus, short crus (related to capsule ) < POSTERIOR
Malleus, SUPERIOR ‘WS
‘Remnant of connection, arches I,Il
INFERIOR
I | Lateral view a
Fig. 6. Despite the fact that the branchial elements remain mesenchymal, several advances have been made between the 9.6-mm. stage and the specimen of 11.7 mm. (6 weeks), the latter here illustrated. The stapedial artery has changed the sta pedial anlage into a ring with the formation of an obturator foramen. (fig. 6a); the interhyale has regressed in size, owing to pressure of the facial nerve; the stapedial anlage and laterohyale become more definite parts of this still membranous visceral bar; the primary continuity between the visceral bars is lost as a separation of the interbranchial bridge from the second visceral bar is completed through the influence of the chorda tympani (compare fig. 5); ‘a groove in the mesenchymal mass between the arches (still continuous with the first visceraltar) has developed at right angles to the first bar, initiating separation of the primordium of the incus from that of the malleus (fig. 6c); a secondary continuity between the first two arches is established as the anlage of the incus approximates the stapedial ring, a relationship which serves to identify the capital part of the primitive stapes. HANSON ET AL.—AUDITORY OSSICLES 367
Embryo, 14mm.
a REICHERT’S CARTILAGE
- Hyoid blastema
[Anterosuperior view] ‘
MECKEL’S CARTILAGE
b.
--Stapes
~~Incus, malleus
I
Posteroinferioy view
SUPERIOR I «Malleus St Incu eros ANTERIOR POSTERIOR ¥ Interhyale Remnant of [Lateral view | a, a INFERIOR
Fig. 7. In the embryo of 14 mm. (6% weeks), although general advancement in development is evidenced, the stapes has not attained the form of a ring; it has been grooved by the artery, but has assumed the form of a horseshoe. This observation would indicate a congenital origin for the excessively thinned and malformed ossicles frequently seen during endaural surgery.
The interbranchial bridge remains on the right side, but the continuity on the left side is broken; only a remnant of this connection remains (fig. 7c). The interhyale is a rather prominent link between the stapes and the hyoid bar (fig. 7a). A groove has begun to separate the malleus from the incus, but the latter is not yet in contact with the stapes. 368 QUARTERLY BULLETIN, N.U.MLS.
Embryo, 15.5mm.
a. -REICHERT’S CARTILAGE Hyoid arch }
!
laterohyalg
Interhyale » Stapes
|Anterosuperioy view
MECKEL’S CARTILAGE
to.
Interhyale -
SUPERIOR
Cc: I Incus
-Malleus
POSTERIOR
ANTERIOR eas
lateral view] 1 PY ncrnyale
INFERIOR
Fig. 8. In an embryo of 15.5 mm. (61 weeks) the annular stapes remains in continuity with the
hyoid bar through the membranous interhyale as a connecting link. Although reduced somewhat in thickness, the interhyale has increased in cellular density.
Only a slight thickening in the hyoid bar remains to serve as a reminder of its primary continuity with the mandibular bars, the blastemal mass itself having differentiated into mesenchymal “models” of the malleus and incus. The position of the chorda tympani serves to render distinguishable the primordial parts for the manubrium of the malleus and the long crus of the incus; they are not yet wholly separate, because loosely arranged mesenchyma bridges the gap between the more densely packed structures. The body of the incus and the head of the malleus are not histologically separated, but a circumferential sulcus is indicative of the site of the future incudomalleolar joint.
A secondary continuity between the visceral bars is maintained by the incudostapedial union. The mesenchymal cells of their anlagen blend in such a manner as to obscure the margins, a circumstance which supports the concept that the long crus of the incus and the stapedial ring develop from a common source, namely, the second visceral arch. HANSON ET AL.—AUDITORY OSSICLES 369
Anterior 155 mm. cardinal vein /
Auricle.
(primordium)
Laterohyale ~a
Stapedial
nerve —— fe SAS Sa : — artery ps
1 Eaed ti lygephetic
Otic capsule
Fig. 9. The precartilage stage is reached in the embryo of 15.5 mm. (7 weeks). However, only the distal portion of the first and second visceral bars are so advanced; the proximal portions of both bars and the primordia of the ossicles are still composed of condensed mesenchyme (more compact than in the previous stage). The stapes is now definitely annular in form, with a distinct ebturator foramen whose margin is separated from the contained stapedial artery by a less dense zone of mesenchyme. :
The crura of the stapes are round in cross-section. The stapes itself is annular. The medial part seems to be imbedded in the precursor tissue (precartilage) of the developing otic capsule. It is as if this annular collection of cells, by pressing inward against the otic capsule, were causing capsular cells to condense in the territory of the future lamina stapedialis (which will contribute to the base of the stapes and the annular ligament).
The facial nerve passes between the laterohyale and the stapedial ring just above the level of the interhyale. The laterohyale and the short crus of the incus (that is, its mesenchymal forerunner) end freely in loose mesenchymal tissue; they are not yet in contact with the otic capsule. In the period between this and the preceding stage the interhyale has undergone further decrease in size. 370 QUARTERLY BULLETIN, N.U.MLS.
Twk. (17mm.)
a. Site of upper attachment of Reichert’s cartilage (lat.hyale Reichert’s cartilage Leper region ) ea
| 4 Primordium of
<~ stapedial muscle
e Gnterhyale region )
Base ~” of stapes
Meckel’s cartilage ““a | Anterosuperior view |
Ossification center of mandible
>--Ossification center (mandible)
Posteroinferior view
Fig. 10. By the 17-mm. (7-week) stage, the mandibular and hyoid bars have developed into cartilage through the greater fraction of their length, and hence may be properly termed Meckel’s and Reichert’s cartilages. The proximal extremity of each bar and the ossicles are still composed of precartilage; however, the malleus and incus are more distinctly outlined — and less a part of the mesenchyma from which they were derived.
The laterohyale and the short crus of the incus approximate and fuse to the under surface of the developing capsule between the 15.5 and 17-mm. stages (fig. 10a, at reader's left). The secondary nature of this continuity with the developing capsule means that the capsule makes no contribution to these primordia.
Concurrently, ossification centers for the mandible appear as membrane bone, one on each half, formed at the distal end of the mandibular arch, HANSON ET AL.—AUDITORY OSSICLES 371
17 mm. REICHERT’S
t CARTILAGE
(Branchial arch Il) filial
aS Interhyale t INCUS
Otic —4
Fig. 11. Although the interhyale has become considerably narrower in the embryo of 17 mm. (? weeks), it still serves as a definitive connection between the visceral bar (Reichert’s cartilage) and the stapes. The second visceral har may be regarded as bifurcating at its proximal extremity, the divergent parts continuing as the laterohyale and the interhyale, with the facial nerve passing over and between them. The laterohyale is now continuous with the capsule and the interhyale is (as it was from the beginning) continuous with the stapes. The size, shape and relationships of the interhyale have changed markedly since its differentiation from the blastemal lobe of the 7-mm. embryo; its mesenchymal composition has not yel been altered, despite the fact that it will soon assume the role of tendon for the stapedial muscle.
The otic capsule, continuing its increase in size, shows transition from mesenchyme to precartilage to cartilage. The stapedial impression into the capsular wall is thus increased by differential growth, but the division between the annulus stapedialis and lamina stapedialis remains apparent. The cells of the stapes, however, blend with those of the incus, there being no articulation as yet at the incudostapedial junction.
A small stapedial artery (arrow) is seen medial to the stapedial ring; it can be traced through the obturator foramen. to its source lateral to the ossicle. tr
QUARTERLY BULLETIN, N.U.M.S.
Embryo, 21mm.
a. _Stapedial muscle
y Laterohyale
p mee Facial nerve
u
Chorda tympani¥> J \ Malleus
Mandible
[Anterosuperior vie
YW b Laterohyale MECKEL’S CARTILAGE ptapedial muscle
wz
MA 1 ate . ‘ : I x
oe . ~® Hyoid cartilage |
i \ i Mag
| Posteroinferior view
SUPERIOR
Cc. a
Malleug Incus ‘Tateral view I Facial nerve [ tateral_ view 4 Chorda tympani, 5 e ANTERIOR POSTERIOR
- . Stapes
I 4 t at ape nial muscle Laterohyale
INFERIOR
Fig. 12. In the embryo of 21 mm. (72 weeks) the ossicles are almost entirely cartilaginous. The mandible, formed in membrane bone, is now two-thirds as long as the branchial arch which it will ultimately replace.
A condensation of cells dorsomedial to the facial nerve can be traced upward to join with the interhyale, where the latier departs from Reichert’s cartilage; the interhyale, in turn, is connected with the stapes at the point of its future articulation with the stapes (compare figs. 18 and 19). This condensation is apparently an outgrowth of mesenchymal cells from the interhyale, hence, the primordium of the stapedial muscle (the interhyale itself developing into the tendon of the muscle). HANSON ET AL.—AUDITORY OSSICLES 373
28mm. ‘Tensor tympam
Fig. 13. At approximately the 28-mm. stage the embryo passes into the fetal phase of its developmental history. The cartilaginous ossicles have become clearly predictive ‘‘models” of the adult structures, except for the retention of two embryonic features: the broad connection between the malleus
and Meckel’s cartilage and separateness of the anterior process.
muscle — (primordium);
Fig. 14. By the 28-mm. stage (8/2 week), the cartilaginous ‘“‘models”’ of the ossicles resemble adult structures; formative steps in development have been taken and primitive branchial relationships have been lost —- the latter fact serving to emphasize the importance of studying very young embryos.
The sulcus which will become the facial canal is partially closed laterally by the laterohyale (proximal portion of Reichert’s cartilage) where it fuses with the otic capsule. This portion of the cartilaginous bar remains an important parietal element up to the 24-week stage, when it begins to become incorporated in the lower part of the definitive facial canal. Eventually the entire laterohyale becomes ossified and loses its identity in the wall of the adult facial canal.
The primordium of the stapedial muscle occupies a position in the sulcus which becomes the facial canal, lying medial to the nerve. The canal is relatively small and the contents are closely confined therein (see fig. 15 for the opposite, or ossicular extremity of the stapedial muscle).
The tympanic cavity is expanding, from the lateral end of the auditory tube, to invade the primitive mesenchymal tissue. The tympanic mucous membrane will invest the ossicles and cover the entire contents of the middle ear as the cavity enlarges.
The chorda tympani branches from the facial nerve below the laterohyale and courses upward to pass between the manubrium of the malleus and the long crus of the incus (compare fig. 13) and therefrom into the mandibular arch. 374 QUARTERLY BULLETIN, N.U.M.S.
Fig. 15. Ata more cranial level than that shown in Figure 14, the interhyale (tendon of the stapedial muscle) inserts into the head of the stapes (where the articulation will later be formed). The course of the stapedial muscle can now be traced from its source in the primitive facial canal, to the angle in Reichert’s cartilage where the laterohyale begins; then upward and forward as the laterohyale, through the loose mesenchyme of the middle ear; finally to an insertion into the posterior aspect of the head of the stapes. At the stage here illustrated the primordium of the stapedial muscle and its tendon are still in approximation with Reichert’s cartilage.
The stapes is impinging on the cartilaginous otic capsule. This area of compact tissue (*) serves to identify the developing lamina stapedialis at the site of the future vestibular fenestra (oval window). The capsular tissue contributes to the base of the stapes and to the annular ligament, by which the stapes will be held within the capsule in later stages. The vestibular aspect and fenestral surface of the base will retain this cartilaginous lamina throughout the individual's lifetime, as will, likewise, the periphery of the fenestra, HANSON ET AL.—AUDITORY OSSICLES 37
way
Fetus, 8/2 WEEKS
Dural venous
--—-4--— sinus
i
Brain ~
Meningeal _ Posterior tissue _—semicircular can
Otic capsule _——Utricle cartilage e
at oo | Lateral . on rE BA: semicircular
Ge 3 < e ee a duct Periotic tissue ~~ i eet ——~ Facial nerve
(future scala) Cochlear duct-# Auditory tube +
— = plate for
Internal extern terydgoid — acoustic meatus muscle ~-~~.Tympanic rin MECKEL'S- \ Gas fae CARTILAGE "ee center) (Branchial ay’ Po
arch L) cA
Masa Mass eter
muscle
o Integument
Fig. 16. Other important changes have taken place in the 28-mm. fetus. The cartilage of the otic capsule is deorganizing around the endolymphatic spaces to become periotic tissue, from which the future vestibular and tympanic scalae will be formed. This process has progressed more rapidly in the region of the cochlea than in the canalicular region. The stapedial impression on the capsular wall, between capsular and tympanic subdivisions, identifies the developing lamina stapedialis (capsular contribution of the base).
The auditory tube is extending into the region of the future middle ear medial to the manubrium of the malleus; its mucous membrane will thus expand to become that of the tympanic cavity.
Meckel’s cartilage now lies medial to the ossifying mandible with the closely associated masseter muscle and lateral to the internal pterigoid muscle. The cartilaginous bar passes up toward the malleus, with which it is still broadly connected (fig. 13).
The anterior process (not seen at this level) and tympanic ring make their first appearance at this stage in the form of ossification centers of membrane bone.
The ectodermal plate for the external acoustic meatus approaches the lateral aspect of the manubrium of the malleus, where it will meet the mucous membrane of the tympanic cavity and the intervening connective tissue (derived from the mesenchyma) to form the tympanic membrane. 376 QUARTERLY BULLETIN, N.U.M.S.
FETUS, 9 WEEKS MIDDLE EAR 40 mm. Tympanic cavity uditory ossicles
Cranial cavi
Chondrocranium——==4 Grain excised)
EXTERNAL EAR “Auricle
be --Cartilage i
PD: caren (earaordicr)
Ne
INTERNAL EAR 3 Otic labyrintha== Periotic labyrinth—— (future vestibule) @xic capsule-~ RE LATED STRUCTURES ~_~—--Condyle ~-~-Coronoid process
RELATED fe STRUCTURES "A “\
Meckel’s cartilage-* --~ 3 te lee ———— Palate uditory tube ae NVA BC 77 ----- Body of mandible nerynx (nasal) ---~ 5 ——- ----- Nasal concha o ; / if Integumentum Nares Nasal septum (cartilage)
Fig. 17. In the fetus of 40 mm. (9 weeks) all structures which will become part of, or related to, the ear of the adult, are present in a stale of recognizable incipiency.
The cartilaginous otic capsule is a preosseous element of the chondrocranium; within it the reticular tissue, which replaced precartilage, has in turn been resorbed to produce the intercommunicating system of the perilymphatic (periotic) labyrinth. Lodged within this labyrinth is that of epithelia ducts, the endolymphatic (otic) labyrinth.
The parts of the adult external ear are represented by the auricle (in which cartilage is already developing) and by the primordial stalk of ectoderm which, upon rearrangement and disappearance of cells, will become the external acoustic meatus.
In the middle ear the auditory ossicles are lodged in primitive mesenchymal tissue; they are still wholly cartilaginous, and will remain so until the fetus has reached the 117-mm. stage, at which time ossification appears first in the incus.
The facial canal and the primordium of the stapedial muscle have changed little since the 28-mm. stage, advancement being limited to separation of the stapedius from the source-structure, the laterohyale. Segregation is complete in the 43-mm. fetus, and conversion of the undifferentiated mesenchymal cells of the laterohyale into muscle tissue is under way.
In specimen of the same age, fibers from the facial nerve pass to the muscle blastema — an observation which led some investigators to conclude that innervation bu this nerve from the second arch spelled origin of the stapes from the same branchial source. HANSON ET AL.—AUDITORY OSSICLES 377
Be ise, as r edie of ™ pista: edial
- 3
Vestibul Fig. 18. In the 21-week stage the ossicles are still cartilaginous al the insertion of the tendon and the incudostapedial joint is still mesenchymal. The ossification center in the slapes is advancing toward the head, having already converted the crura and the tympanic part of the base into perichondral bone.
The stapedial tendon is inserted into both the long crus of the incus and the head of the stapes (an arrangement which was encountered in 30 of 198 series, fetal and adult). 378 QUARTERLY BULLETIN, N.U.M:S.
Tendon of
stapedial .
muscle.=
membrane. 4
te
iL
Fig. 19. In the newborn the ossicles are, in all major features, adult elements of the human skeleton. The stapes, for example, retains a mere remnant of its fetal structure, namely marrow limited to the
interior of the cervical and capital parts and to the inner circumference of the base.
Evident likewise in this and many other postnatal specimens (including some to the age of 70 years) is the occurrence of double insertion of the stapedial tendon. This. means that the early association with the incus (compare fig. 18) is not lost as the ossicles mature and as the incudostapedial joint
is formed.
These observations are interpreted to mean that the manubrium of the malleus and long crus of
the incus, as well as the greater part of the stapes, are derived from the second branchial arch. HANSON ET AL.—AUDITORY OSSICLES 379
-Anterior
process of
malleus
yf —- 1 f > itis. | 78 aul
Fig. 20. In the fetus of 161 mm. (19 weeks) Meckel’s cartilage is beginning to undergo ossification near the zone in which altered tissue will differentiate into that of the anterior ligament of the malleus (fig. 20a). Three weeks later, in the fetus of 190 mm. (22 weeks) the anterior process of the malleus has become attached to the neck of the ossicle (fig. 20b, at arrows).
In the 215-mm. (24-week) stage, Reichert’s cartilage, continuous with the otic capsule, forms part of the wall of the facial canal (fig. 20c). In early infancy, the cartilage (a derivative of the laterohyale) is a mere remnart (fig. 20d). Newly-formed membrane bone and expanding tympanic cavity
(at : in both figs. 20c and 20d) intervene between the contents of the canal and the residual, invested, cartilage.
. #Tympanic cavit
ie
