Paper - The development of the otic capsule in the region of the vestibular aqueduct

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Anson BJ. and Bast TH. The development of the otic capsule in the region of the vestibular aqueduct. (1951) Q Bull Northwest Univ Med Sch. 25(2): 96-107. PMID: 14834339.

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This historic 1951 paper by Anson and Bast described the human otic capsule in the region of the vestibular aqueduct.


See also: Anson BJ. and Bast TH. The development of the otic capsule in the region of the vestibular aqueduct. (1951) Trans Am Otol Soc. 39(84th Meeting): 97-109. PMID: 13005605.
Also by this author:

Bast Selected References 
Theodore H. Bast
Theodore H. Bast (1890-1959)

Bast TH. The utriculo-endolymphatic valve. (1928) Anat. Rec. 40, 110. 1: 61-64.

Bast TH. Development of the Otic Capsule I. Resorption of the cartilage in the canal portion of the otic capsule in human fetuses and its relation to the growth of the semicircular canals. (1932) Arch. Otolaryng. 16:19

Bast TH. Development of the otic capsule II. The origin, development and significance of the fissula ante fenestram and its relation to otosclerotic foci. (1933) Arch. Otolaryng. 18(1):

Bast TH. Development of otic capsule III. Fetal and infantile changes in fissular region and their probable relationship to formation of otosclerotic foci. (1936) Arch. Otolaryng. 23: 509-525.

Bast TH. Development of otic capsule IV. Fossula Post Fenestram. (1938) Arch. Otolaryng. 27: 402-412.

Bast TH. Ossification of the Otic Capsule: in Human Fetuses. (1939) Contrib. Embryol. (no 121) 21: 52-93.

Bast TH. Development of the Otic Capsule: II. The Origin, Development and Significance of the Fissula Ante Fenestram and Its Relation to Otoscerotic Foci. (1939) Arch. Otolaryng. 18: 1-20.

Bast TH. Perichondrial ossification and the fate of the perichondrium with special reference to that of the otic capsule. (1944) Anat. Rec. 90(2): 139–148.

Bast TH. Development of the aquaductus cochleae and the periotic (perilymphatic) duct. (1946) Anat Rec. 94: 449. PMID: 21020575.

Bast TH. Development of the aquaeductus cochleae and its contained periotic duct and cochlear vein in human embryos. (1946) Ann Otol Rhinol Laryngol. 55: 278-97. PMID: 20993452.

Anson BJ. Cauldwell EW. and Bast TH. The fissula ante fenestram of the human otic capsule; aberrant form and contents. (1948) nn Otol Rhinol Laryngol. 57(1): 103-28.PMID: 18913523.

Anson BJ. Bast TH. and Caudwell EW. The development of the auditory ossicles, the otic capsule and the extracapsular tissues. (1948) Ann Otol Rhinol Laryngol. 57(3):603-32. PMID: 18885441.

Book - Bast TH. and Barry J. Anson. The temporal bone and the ear. (1949) (1st ed.) Springfield, Ill. C.C. Thomas, 478 pages.

Anson BJ. and Bast TH. The development of the otic capsule in the region of surgical fenestration. (1949) Q Bull Northwest Univ Med Sch. 23(4): 465-77. PMID: 18148737.

Anson BJ. and Bast TH. The development of the otic capsule in the region of surgical fenestration. (1949) Ann Otol Rhinol Laryngol. 1949 Sep;58(3):739-50. PMID: 15397200.

Bast TH. and Anson BJ. Postnatal growth and adult structure of the otic (endolymphatic) sac. (1950) Ann Otol Rhinol Laryngol. 59(4): 1088-1101.PMID: 14800237.

Anson BJ. and Bast TH. The development of the otic capsule in the region of the vestibular aqueduct. (1951) Q Bull Northwest Univ Med Sch. 25(2): 96-107. PMID: 14834339.

Bast TH. and Anson BJ. The development of the cochlear fenestra, fossula and secondary tympanic membrane. (1952) Q Bull Northwest Univ Med Sch. 26(4):344-73. PMID: 13004246.

Richany SF. Bast TH. and Anson BJ. The development of the first branchial arch in man and the fate of Meckel's cartilage. (1956) Q Bull Northwest Univ Med Sch. 30(4):331-55. PMID: 13408429.

Anson BJ. and Bast TH. and Richany SF. The development of the second branchial arch (Reichert's cartilage), facial canal and associated structures in man. (1956) Q Bull Northwest Univ Med Sch. 30(3): 235-49.PMID: 13359646.

Anson BJ. and Bast TH. Anatomical structure of the stapes and the relation of the stapedial footplate to vital parts of the otic labyrinth. Trans Am Otol Soc. 1958;46:30-42. PubMed PMID: 13793785.

Anson BJ. and Bast TH. Development of the otic capsule of the human ear; illustrated in atlas series. (1958) Q Bull Northwest Univ Med Sch. 32(2):157-72. PMID: 13554750.

Hanson JR. Anson BJ. and Bast TH. The early embryology of the auditory ossicles in man. (1959) Q Bull Northwest Univ Med Sch. 33: 358-379. PMID: 14399619

Anson BJ. and Bast TH. Development of the incus of the human ear; illustrated in atlas series. (1959) Q Bull Northwest Univ Med Sch. 33(2): 110-9. PMID: 13668024.

Stelter GP. Bast TH. and Anson BJ.The developmental and adult anatomy of the air-cells in the petrous part of the temporal bone. (1960) Q Bull Northwest Univ Med Sch. 34: 23-37. PMID: 13834276.

Also by related authors:

Anson BJ. Karabin JE. and Martin J. Stapes, fissula ante fenestram and associated structures in man: I. From embryo of seven weeks to that of twenty-one weeks (1938) Arch. Otolaryng. 28: 676-697.

Anson BJ. Karabin JE. and Martin J. Stapes, fissula ante fenestram and associated structures in man: II. From Fetus at Term to Adult of Seventy (1938) Arch. Otolaryng. 28: 676-697.

Beaton LE. and Anson BJ. Adult form of the human stapes in the light of its development (1940) Q Bull Northwest Univ Med Sch. 14(4): 258–269. PMC3802306

Cauldwell EW. and Anson BJ. Stapes, fissula ante fenestram and associated structures in man III. from embryos 6.7 to 50 mm in length. (1942) Arch. Otolaryng. 36: 891-925.

Anson BJ. and Cauldwell EW. Stapes, fissula ante fenestram and associated structures in man: IV. From fetuses 75 to 150 mm in length. (1943) Arch. Otolaryng. 37: 650-671.

Hanson JR. and Anson BJ. Development of the malleus of the human ear; Illustrated in atlas series. (1962) Q Bull Northwest Univ Med Sch. 36(2): 119–137. PMID: 13904457.



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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


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The development of the otic capsule in the region of the vestibular aqueduct

Barry Joseph Anson
Barry Joseph Anson (1894-1974)
Theodore H. Bast
Theodore H. Bast

Barry J. Anson and Theodore H. Bast

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Introduction

General aspects of the authors’ inclusive otological study have already been reported at successive annual meetings of the American Otological Society and subsequently recorded in a series of journal articles (see References). They were concerned with the developmental and adult anatomy of the auditory ossicles, of the otic capsule and extracapsular tissues, of the endolymphatic sac, and of the capsular wall of the lateral semicircular canal in the region of surgical fenestration. In the present article the authors will review the major features in the morphogenesis of another special portion of the otic capsule. The observations herein recorded are based upon an examination of a large number of series of sections in the otological collection at the University of Wisconsin. Representative specimens were selected for description; of these, 7 were taken for illustration, in figures which will serve as the chief basis for the observations recorded in the text.

The writers have already established the fact that maturity in gross form and size and in histological structure is at ‘From the Department of Anatomy of Northwestern University Medical School (Contribution No. 571) and the Department of Anatomy of the University of Wisconsin. This study was conducted under the auspices of the Central Bureau of Research of the American Otological Society.

Paver read at the Eighty-fourth Annual Meeting of the American Otological Society, Atlantie City, May 11-12, 1951, and at the Sixty-seventh Annual Meeting of the American Association of Anatomists, Detroit, March 21-23, 1951. Received for publication, March 21, 1951.

At the five preceding meetings of the American Otological Society (1946-1950) the authors presented papers dealing with the development of the auditory ossicles, of the fissula ante fenestram and of the otic capsule and extracapsular tissues. These have appeared in six articles in the Annals of Otology, Rhinology and Laryngology (see References). Other articles on similar and related subjects, by the authors and their colleagues, have appeared in the above-named Journal (53:42-53, 1944; 51:343-357, 1942; 57 :891-904, 1942), in the Arch. Otolaryng. (37:650-671, 1943; 28:676-697, 1938; 29:939-973, 1939; 30:922-942, 1939: 27 588-605, 1938; 10:459,-471, 1929; 16:19-38, 1932; 18:1-20, 1933 ; 23:509-525, 1936; 27 :402-412, 1938; 32:771-782, 1940; 30:183-205, 1939; 36:891-925, 1942); in the Laryngoscope (56 :561-569, 1946); in the Quart. Bull. Northwestern Univ. Med. School (14:250-257, 1940; 15:258-269, 1941; 18:33-40, 1944; 23:465-477, 1949); and in the Contrib. Embryol, Carnegie Institution (21:53-82, 1930).


tained by the otic capsule, as well as by the auditory ossicles and membranous labyrinth, far earlier than was once believed, and in ways that mark it as the most highly specialized element of the human skeleton.

As pointed out in antecedent articles, in the surgically important region of the otic capsule, that is, the tympanic wall of the lateral semicircular canal, the process of ossification is, in the early stages, essentially the duplicate of that which operates to form any typical portion of the capsule. However, at approximately the stage of midterm, the process of ossification in the region of surgical fenestration begins to follow a special course. Within a period of four weeks thereafter, the recently formed outer (periosteal) layer has been largely removed. So rapid is this process of resorption that soon varying amounts of the middle layer (endochondral bone and the cartilage islands) are likewise destroyed. Following this stage of resorption, during the progress of which tympanic air-cells are abortively formed, new bone is added on the tympanic surface, to restore a smooth contour. As a consequence, the mucoperiosteal membrane covers this secondary bone, instead of the original periosteal layer. In this way, the tympanic wall of the lateral canal, after having been eroded deeply on the external aspect, is rebuilt to assume regular structure and thickness.


In the current report, consideration will be given to the development and adult structure of the opposite (medial) wall of the capsule, in the territory of the cranial orifice of the vestibular aqueduct and the adjacent portion of the posterior surface of the petrous pyramid. Rarely the site of pathological tissues, this area undergoes a series of morphogenetic changes resembling those by which the tympanic wall of the lateral semicircular canal is formed, then resorbed, and finally rebuilt.


It is important to point out that, of the three histologically active areas, only the fissular region is a common site of continuing instability and of pathogenetic activity. Once reconstructed, the two walls remain quiescent; on the contrary, the intracapsular tract of the fissula ante fenestram may harbor a chondroma, osteoid tissue—or even sclerotic bone.

Observations and Discussion

The otic capsule differs from all other skeletal elements of the human body in respect to function, rapidity of development, mode of ossification and histologic fabric. Actually, in every phase of the otological investigation the authors have been surprised by the unique character of capsular fabric and by the manner of its genesis.


The development of the capsule is rapid; it attains adult dimensions when the fetus reaches the middle of its intrauterine existence. In contrast, a typical long bone continues to grow through a period of twenty or more years. Although the otic capsule retains fetal dimensions throughout life, it does acquire a thick investment of extracapsular periosteal bone, and, as a consequence, becomes the labyrinthine core of the so-called petrous pyramid. The structure of the otic capsule is unique, also, in being formed from fourteen primordially independent ossification centers. Bone spreads from each of these originally separate centers, not, as in a typical long bone, from a point of initial ossification in the middle of a diaphysis toward terminal epiphyses. Fusion between centers is peripheral and complete; there exist no zones of secondary, or epiphyseal growth such as regularly occur in a long bone. Fusion, with complete erasure of fusion-lines between contiguous centers, early converts the otic capsule into an osseous unit. Histologically, too, the otic capsule is exceptional. In the antral region of the capsule, the outer one of its three capsular layers become pneumatized throgh invasion by mucuos membrane. The middle layer, most complex of the three, retains throughout life a considerable fraction of its primitive cartilage in the form of chondral islands lodged in endochondral bone; this layer of dual origin is never converted into haversian bone. The inner layer is simplest; it forms a thin, but unchanging, shell for the labyrinthie canals, the cochlea and the vestibule. The layer fuses with the endochondral bone of the middle layer.


The periosteal (or external periosteal) layer forms a complete outer shell earlier in the cochlear than in the canalicular division of the capsule. This outer layer is destined to produce all of the extracapsular tissue; as a result of its thickening, through the activity of the investing periosteum, the adult dimensions of the temporal bone will be attained. While its bulk is being thus increased, the original labyrinthic capsule (bounded by the endosteal layer) undergoes no enlargement; its fetal size is maintained unaltered in the adult.


The endosteal (or internal periosteal) layer, produced by the periosteum on the inner surface of each of the several ossification centers, forms a thin wall for the labyrinthic spaces. Production of this layer is begun in the fetus of 150 mm. (11 weeks); it is complete within a 3-week period (in the 183-mm., 21-week, stage), except where it constitutes the peripheral portions of the semicircular canals.


As mentioned briefly above, the middle layer is made up of two kinds of osseous tissue. The intrachondral bone appears before the endochondral. The former is present in the fetus of 120mm. (16 weeks) ; attaining maximum development in the fetus of 183 mm. (21 weeks), the intrachondral bone (cartilage islands) never wholly disappears. Although in some regions of the capsule the cartilage islands may be destroyed, in other parts they seem to be as abundant in the adult temporal bone as they were in that of the midterm fetus. Soon after the chondral islands attain widespread distribution in the capsule, the formation of endochondral bone is initiated; the latter is a new tissue, deposited by osteoblasts upon the islands of calcified cartilage (fig. 1, inset). The speed of deposition of the endochondral bone differs in the several subdivisions of the capsule; once formed, neither the cartilage islands nor the layers of endochondral bone in which they become imbedded are ever replaced by haversian bone.



Fig. 1. Photomicrograph of a transverse section through the otic capsule at the level of the cranial orifice of the vestibular aqueduct in a fetus of 150 mm. CR length (181% weeks). Wisconsin ser. 39, slide 26, section 1. X 28.

On the medial wall of the cranial orifice, the cartilage is still unmodified; on the lateral wall, ossification has been initiated (forming Center 10 of Bast’s description). In this area the cartilage is being converted into intrachondral bone; in later stages in the process of ossification, the primordial cartilage will persist, to appear as islands of modified cartilage in a field of mature bone. In the region illustrated neither periosteal (outer periosteal) nor endosteal (inner periosteal) bone has yet formed.

Inset: Tissue of the ossification center; detail of the area outlined. X 84. Abbrev., I.b., intrachondral bone in the initial stage of formation.



Fig. 2. Photomicrograph of a section which passes transversely through the cranial orifice of the aqueduct in a fetus of 160 mm. (19% wks.) Wis. ser. 41, sl. 11, sect. 5. X 28.

Bone has been formed on the medial wall; toward the dura, the thin layer is periosteal bone (layer 1) whereas toward the space of the aqueduct the somewhat thicker, irregular, stratum (layer 2) is composed of intrachondral islands upon which the endochondral bone will later be deposited. On the opposite, or lateral, wall of the aqueduct, the tissue is similar to that just described (that is, layer 2). The latter merges with the thin stratum of endosteal (inner periosteal) bone (layer 3) which constitutes the osseous boundary of the labyrinth.


Fig. 3. Photomicrograph of a transverse section through the capsule at the level of the cranial (dural) aperture of the vestibular aqueduct in a fetus of 183 mm. (21 wks.; approximately midterm). Wis. ser. 21, sl. 26, sect. 1, X 28.

In the area of the ossification center (compare fig. 1), endosteal bone is being deposited upon the islands of cartilage; the combined tissue constitutes the middle layer (layer 2) of the otic capsule, which here, not yet covered by periosteal bone, is exposed to the dura mater in the fovea for the otic (endolymphatic) sac. Periosteal bone (at 1) is present as a thin plate on the medial (cranial) surface of the ledge (as far as the unnumbered arrow). The orifice of the aqueduct, early formed in cartilage (fig. 1), now consists of osseous walls and a core of sparsely distributed intrachondral bone. Endosteal bone (at 3), forming the wall of the vestibule (as it serves, also, for other portions of the labyrinth), has already become fused with the adjacent portion of the middle layer.

Inset: Tissue of the middle stratum (layer 2), as it occurs on the lateral wall of the cranial orifice of the aqueduct; detail of the zone outlined in the main figure. X 84. The spicules shown are made up of rapidly growing endochondral bone. The layer is not a continuous sheet; it is, on the contrary, interrupted peripherally by hiatuses through which the developing dura mater meets the primitive marrow of the otic capsule. Abbrev., ost., osteoblasts.


In the region of the cranial orifice of the vestibular aqueduct and in that of the adjacent fovea for the otic (endolymphatic) sac, formation of an outer layer of bone is delayed. To the morphogenesis of this part of the otic capsule, the discussion will now be devoted.

In the 50-mm. (10-week) fetus, the otic capsule has but recently become a definitely bordered cartilaginous unit.'

3In addition to the several stages described in the text and illustrated by figures, 15 others were carefully ex amined for comparative results. These series deserve passing mention.

In the following series, neither described in the body of the text nor employed for illustration, growth of the capsule or differentiation of the constituent cartilage led to the stage of morphogenesis represented by the 150-mm. fetus: 25 mm. (8 wks.), 111 mm. (15 wks.), 112 mm. (15 wks.), 117 mm. (16 wks.), 126 mm. (1614 wks.), and 135 mm. (17 wks.).Comparably, in the fetuses of 170 mm. (20 wks.),

The course of the vestibular aqueduct in the 50-mm. fetus predicts that of the channel in the later stages; it passes obliquely from a vestibular to a cranial aperture. From the cochlear portion of the capsule, the prominent medial wall extends as a short, yet relatively bulky, ledge.

In the 100-mm. (14-week) fetus, the cartilaginous capsule is appreciably larger than it was in the preceding stage. With general growth has come marked elonga175 mm. (20 wks.) and 180 mm. (21 wks.), the stages of development are progressively antecedent to that described for the 183-mm. (21-wk.) fetus. Fetuses of 222 mm. (25 wks.) and 240 mm. (27 wks.) are similar to those of 210 mm. (23 wks.) and 215 mm. (24 wks.) in respect to formation of bone in the region of the vestibular aqueduct. In the 275-mm. (30-wk.) and 290-mm. (32-wk.) fetuses, the capsular wall in the region of the vestibular aqueduct is structurally similar to that in the fetus of 270 mm. (30 wks.) The term fetus, the infant of 4 weeks and the infant of 6 months are not unlike the infant of 10 weeks in respect to the feature of rebuilding of the aqueduct and fovea.


Fig. 4. Photomicrograph of a section passing through the orifice of the aqueduct in a 210-mm. (23-wk.) fetus. Wis. ser. 51, sl. 24, sect. 1. X 28. Near the superior limit of the orifice, membrane bone now covers a portion of both walls of the vestibular aqueduct. The ledge itself, therefore, consists, from the medial to the lateral aspect, of a thinned periosteal stratum, endochondral bone in the form of ‘‘spicules,’ (at 4); the latter ends at the unnumbered arrow.


and newly-formed membrane bone

Inset: Detail of the structure of the ledge in the area outlined (layers numbered). X 84.

tion of the ledge-like medial wall of the vestibular aqueduct. The newly-formed prolongation may show incomplete chondrification in the area over the greatest bend of the aqueduct. That is, incidentally, the area which remains thin and cartilaginous in the fetus of 160 mm. (1914-week stage), when surrounding tissue has become ossified (fig. 2).

In the fetus of 150 mm. (1844 weeks) an ossification center has appeared on the lateral wall of the vestibular aqueduct (fig. 1). Within the ossifying area, intrachondral bone is being formed, as the primary tissue of the middle layer; neither periosteal nor endosteal bone has yet appeared, and the medial wall of the orifice of the aqueduct is still cartilaginOUS.


The second important step in the process of ossification of the vestibular aqueduct is evidenced in the fetus of 183 mm. (21 weeks) (fig. 3). Through spreading ossification, the ledge which guards the cranial orifice of the aqueduct now consists of the three typical layers of bone. On the medial wall, the periosteal layer is still thin, as is also the endosteal (at 3), where the latter bounds the vestibule. Between these strata, the middle layer (at 2) consists of sparsely distributed intrachondral bone. Proximal to the point at which the ledge becomes continuous (fig. 3, at unnumbered arrow) with the fovea for the otic (endolymphatic) sac, the outer layer ends, to leave the middle layer exposed to the dura mater. The middle layer, except where it constitutes the sparsely occupied core of the ledge, no longer consists solely of intrachondral bone; upon the islands of cartilage, endochondral bone is now being deposited. Ultimately, through continued production of the latter, the intervening marrow spaces will be reduced to small spaces for transmission of the bloodvessels. Generally speaking, the intrachondral bone remains relatively unaltered throughout life; however, in the core of the ledge, the islands of intrachondral bone will be almost completely removed in later developmental stages (see fig. 5).


Fig. 5. Photomicrograph of a transverse section through the otic capsule at a level of the dural (cranial) opening of the aqueductus vestibuli in a 215-mm. (24-wk.) fetus. Wis. ser. 62, sl. 18, sect. 8. X 28.

The outer, periosteal, layer (at 1) has undergone considerable thickening. On the wall of the vestibule the inner, endosteal layer (at 3) is fused with the middle layer of the capsule. The middle layer (at 2) is exposed to the dura mater of the cranial orifice and along the wall of the fovea for the otic sac; it is likewise uncovered at the margin of the ledge. Not only has the middle layer not become wholly covered by periosteal bone (outer layer), but actually is being eroded (see inset). As a consequence, intrachondral bone, once invested by endochondral bone, is now in contact with meningeal tissue. Concurrently, the medial wall of the ledge is receiving a new covering; here membrane bone (at 4) is being deposited upon the formerly irregular surface of the middle layer, as it was in the preceding stage.


Inset: Character of the middle layer, as shown in the typical area, marked out as a rectangle in the main figure. X 84. The ossified cartilage islands (intrachondral bone) persist prominently within the endochondral bone. Their globular character stands in marked contrast with the structure of the osseous tissue in which they have been, and are still being, imbedded.


In the 210-mm. (23-wk.) fetus the results of both erosion and deposition are in evidence (fig. 4). On the medial surface of the ledge (facing the cranial cavity) not only has some of the outer (periosteal) layer been removed, but also a fraction of the underlying middle (endochondral) bone and the contained cartilage islands (fig. 4, inset, at unnumbered arrow). However, on the lateral wall (facing the vestibular aqueduct) membrane bone (inset, at 4) is being deposited upon the middle (endochondral) layer (inset, at 2). Here, near the superior limit of the cranial aperture of the aqueduct—where the ledge merges with the general surface of the petrous pyramid —membrane bone is also present on the medial wall of the aqueduct. Bone of this type has not yet, but ultimately will, spread along the surface of the fovea to cover the now exposed bone of the middle layer. As a result of the application of bone to both aspects of the cranial orifice of the aqueduct and to the neighboring fovea, the previously excavated space will be reduced in capacity to accommodate the otic sac and its investing sheath of dura mater. The structure of the new bone within the aperture of the aqueduct is strikingly different from that of the periosteal bone on the cranial surface of the ledge (figs. 4 to 6); the former is without definite pattern, whereas the latter is strikingly laminar.

In the fetus of 215 mm. (24 wks.) the periosteal layer on the medial (cranial) aspect of the ledge is considerably thicker than it was in the fetus of 183 mm.; the layer gradually thins and finally ends at the tip of the ledge (fig. 5). Within the core of the ledge, the middle layer is almost devoid of cartilage islands; however, in the two remaining thin strata of endochondral bone a few such islands remain. On the lateral aspect of the ledge, one phase of the third in the series of developmental steps is being evidenced: membrane bone (at arrow 4) is being deposited upon the remnant tissue of the middle layer. Another phase is_represented by the erosion of the lateral wall of the fovea and aqueduct; removal of this middle layer includes destruction of the intrachondral bone (inset, fig. 5). Through the operation of these concurrent processes of deposition and erosion, the cranial orifice of the aqueduct and the fovea of the endolymphatic sac are altered in form and size.



Fig. 6. Photomicrograph of:a transverse section through the orifice of the vestibular aqueduct in a fetus of 270 mm. (30 wks.). Wis. ser. 107, sl. 10, sect. 11. X 28.

The ledge of bone has undergone further alteration in form through the production of additional membrane bone (at *). The original periosteal part remains as a slender projection (at 1). Within the orifice, membrane bone (at 4) has enveloped the otic sac, to produce a new, or secondary, cranial opening for the vestibular aqueduct. This layer is spreading along the medial wall, covering bone of the middle layer as it progresses. In the middle layer the persistent cartilage islands remain (lower arrow 2) to, become permanent adult constituents of the capsule.

Inset: Structure of the bone on the lateral wall of the aqueduct in the zone blocked in the main figure. X 84. Abbrev., E.b., endochondral bone; I.b., intrachondral bone; M., marrow.


In the fetus of 270 mm. (30 weeks) the ledge of bone which forms the medial wall of the orifice, at first seemingly com pressed and composed almost wholly of endochondral bone, is now lengthened by the addition of membrane bone, which forms within the excavated, enlarged fovea (figs. 5, 6 and 7). Not only has the new bone (at arrow 4) served to restore the length of the ledge, but also to enclose the otic sac in a less capacious fovea. The membrane bone will continue to spread along the floor of the fovea. The bone of the middle layer, other than that of the ledge, contains prominent islands of intrachondral bone (fig. 6, lower arrow 2) lodged within endochondral bone. The rapid enlargement of the endochondral spicules has been sufficient to reduce the marrow spaces (large in the 215-mm. stage) to channels only slightly more capacious than the blood-vessels which they transmit. The inner (endosteal) layer (at arrow 3) is not as clearly distinguishable from the middle layer as is the new-formed membrane bone. The periosteal layer is thin over the superior portion of the ledge (fig. 6), thick at an inferior level (fig. 7).



Fig. 7. Photomicrograph of a section at a level lower than that in figure 6 (270-mm. fetus, sl. 11, sect. 3), depicting the structure of the capsule around the cranial orifice of the vestibular aqueduct. X 28. At this level (near the inferior limit of the orifice), the periosteal layer (at 1) is thick, the membrane bone (at 4) less well developed. The middle layer (at arrow 2, reader’s right) still constitutes the wall of the aqueduct and fovea.


Formation of membrane bone within the connective tissue of the orifice and fovea continues until the ledge is formed chiefly of that tissue. The result of this alteration is shown in the 10-week infant (figs. 8 and 9). The orifice of the vestibular aqueduct is narrowed, and almost completely filled by the otic sac. On the medial wall of the ledge, the periosteal layer ceases to be readily distinguishable from the original endochondral bone. The same is true of the lateral surface, where the preexisting bone can no longer be distinguished from the new-formed membrane bone. Thus, ultimately, the entire region of the vestibular aqueduct attains the three-layered structure’.

Conclusions

The otic capsule is unique among skeletal elements in respect to several important features, which concern both the morphogenesis of its parts and the character of its constituent tissues. Since some of these features affect the special region of the vestibular aqueduct as well as the capsule as a whole, they may properly be reviewed here, in introduction to the presentations of the authors’ current conclusions.


  • 4 The extended period of development of the capsule in the region of the aqueduct is dependent upon the late expansion of the otic sac. Contrary to older opinion, the endolymphatic (otic) sac in the human ear is so large and capacious that it extends for a relatively considerable distance beyond the cranial orifice of the vestibular aqueduct. Since the greater part of the endolymphatic (otic) sac lies within the substance of the cranial dura mater, its great increase in size causes enlargement of the fovea on the posterior surface of the petrous pyramid. This increase in area accompanies the enlargement of the posterior cranial fossa, whose anterior wall is the petrous pyramid. During this period of growth, the medial margin of the sac retains a close relationship to the sigmoid sinus into which its rich venous plexus drains. The superior boundary of the intracranial portion of this foveate impression is distinct, since it is the semilunar margin of the ledge of bone beneath which the aqueduct opens into the fossa; the inferior boundary may either approach or merge with the sigmoid sulcus.

Since variation in the form, size and distinctness of outline of the fovea in the temporal bone of the adult skull is the rule rather than the exception, comparable difference would be expected between any two fetal or infantile bones studied as serial sections. Consequently, in the specimens described and figured in the present article, the successive steps selected may not exactly duplicate the stages through which any one of the temporal bones would have passed had it been possible to study stages in the morphogenesis of a single ear.


Fig. 8. Photomicrograph of a transverse section through the capsule at the level of the cranial orifice of the aqueduct in an infant of 10 weeks. Wis. ser. 83, sl. 46, sect. 1. X 28.

Periosteal bone (at 1) forms the outer layer of the ledge; the more recently formed membrane bone (at 4) has spread beyond the point reached in the 270-mm. fetus. The new bone lines virtually the entire fovea (compare fig. 7). The steady increase in bulk of the endochondral ‘‘spicules” has resulted in solidification of the capsule to petrous degree and in the consequent reduction in size of the marrow spaces. The orifice of the aqueduct is but little larger than the contained endolymphatic sac. Abbrev.,

Bl.v., blood-vessel.

Developmentally, the capsule represents a fusion of numerous, originally independent, ossification centers. At the time of fusion of the contiguous centers (in the middle of intrauterine life), the labyrinthine spaces thereby enclosed by a thin stratum of bone derived from the inner periosteum, will have attained adult dimensions; subsequent activity of the outer periosteum, while serving grossly to imbed the primordial capsule in the petrous part of the temporal bone, leaves the size of the labyrinth unchanged. The inner periosteal (endosteal) layer is unlike the corresponding stratum of a typical long bone not merely in ceasing to be active in the midterm fetus; additionally, its relationships are of a special order, since it encapsulates a system of interconnected epithelial tubes —cochlear, utriculosaccular, and canalicular. The middle layer of the capsule is also unusual, but in still a different way: structurally, it consists of two dissimilar types of bone, whose initial appearance is not simultaneous and whose periods of maximum growth are not concurrent. Of these two, the tissue consisting of islands of ossifying cartilage is the first to appear; production of endochondral bone soon follows—the latter being deposited upon the cartilage islands (intrachondral bone), to imbed them in “spicules.”” Thickening of endochondral covering, in correspondingly reducing intervening marrow spaces, accounts for the petrous nature of the otic capsule. Once formed, the histologic pattern of the middle layer never changes in normal bone; the combined intrachondral and endochondral bone is never replaced by bone of haversian type.


The series of developmental steps through which the capsule passes in attaining mature form, size and fabric is, to a degree, followed by the capsular wall in the region of the vestibular aqueduct and of the adjacent fovea for the otic (endolymphatic) sac. However, in this territory of the cranial aperture of the vestibular aqueduct and neighboring foveate excavation, the series of changes in the constituent layers depart even more strikingly from the standard pattern of genesis. These steps may be traced in the following selected stages. Late production of an outer layer of bone in this zone is here the result of change in plane of the endolymphatic duct and the enlargement of the endolymphatic sac; to the same causes are owing the histological replacement of some of the tissue of the middle layer. These processes affect the structure of the ledge which, medially, intervenes between the general space of the cranial cavity and the aperture of the vestibular aqueduct, and, concurrently, the structure of the wall which, laterally, intervenes between the aqueduct and the vestibule.



Fig. 9. Photomicrograph of the section shown in Figure 8 (10-week infant), of a more inclusive area of the capsule around the cranial orifice of the vestibular aqueduct. X 15.

The periosteal layer of bone (arrow 1), as it forms the medial wall of the ledge, is indistinctly separated from the endosteal bone (arrow 2). Bone of the latter type is likewise unclearly segregated from membrane bone (arrow 4). Membrane bone has spread beyond the limit of the orifice (that is, past the free margin of the projecting ledge) to provide a new permanent, osseous wall for the fovea of the otic (endolymphatic) sac. The middle layer of bone now consists chiefly of endochondral bone; however, within its substance are contained a considerable number of cartilage islands (intrachondral bone), except in the region of the core of the original ledge, where (as at *) the bone has been removed, then the osseous structure rebuilt. The endosteal layer is, despite its thinness, distinguishable from the middle layer. Virtually unchanged from the time of its full appearance in the 4-month fetus, it forms the wall of the labyrinth (arrow 3).

Arrows from enclosed numerals point to the lines of contiguity of the layers therein numbered.


In the fetus of 18 to 19 weeks (150 mm.) the ledge is still completely cartilaginous; on the lateral wall of the aqueduct an ossification center has appeared.

Within a three-week period (in the fetus of 21 weeks, 183 mm.) the process of ossification has progressed to the point at which the three typical layers have appeared in the greater area of the capsule. However, in the region of the aqueduct, although periosteal bone forms the medial surface of the ledge, bone of endochondral and intrachondral types constitutes the opposite wall. The same middle layer is continued, denuded, along the fovea for the otic sac, in the direction of the lateral venous sinus (that is, away from the orifice of the aqueduct). The endosteal, or inner periosteal layer, which first appeared in the fetus of approximately 19 weeks (160 mm.) is now not only well established, but has virtually attained adult character; forming the wall of the periotic labyrinth, it will be subjected to neither marked histological alteration as a layer nor change in area as the wall of labyrinthic spaces. However, in some specimens the layer fuses so completely with the endochondral bone of the middle layer that the line of original demarcation between them is wholly lost.

Within another three-week period (in the fetus of 24 weeks or 215 mm.) striking changes have occurred in both surfaces of the ledge and along the surface of the fovea. The substance of the original ledge has been almost completely destroyed; the remnants thereof which do persist appear as two thin, facing laminae in which a few cartilage islands are discernible. The medial surface of the ledge is covered by a thick periosteal layer, whereas, on the lateral surface, membrane bone is being deposited. Along the remainder of the wall of the cranial aperture of the vestibular aqueduct and continuously into the fovea, the middle layer of bone remains denuded—being exposed to the dura in which the otic sac is ledged. Here, erosion rather than deposition of bone is occurring; recently exposed endochondral bone has been destroyed, as have also some of the contained cartilage islands—in evidence of a process which transitorily deepens the fovea.

Within 6 weeks, in the fetus of 270 mm. (30 weeks), two changes are evident: the original osseous ledge of bone has become thinner in the remnant middle layer, intrachondral bone having been destroyed; within the orifice, membrane bone envelopes the otic sac, to produce a new or secondary, cranial opening for the vestibular aqueduct. This layer 1s spreading along the medial wall, covering bone of the middle layer as it progresses.

In early postnatal stages (for example, in the 10-week infant), the form and size of the aqueduct and fovea have been profoundly altered: the cranial orifice of the aqueduct, now a crevice (as seen in horizontal sections) is only slightly more capacious than the sac which it contains; the fovea is shallow, that is,no longer an excavated depression. The ledge, whose thickening has taken place at expense of the space over which it projects, now consists of three layers, namely, a relatively thin periosteal layer, an endochondral layer, and a thick stratum of membrane bone. A relatively consider able distance now separates the middle layer of the capsule from the space of the orifice of the aqueduct; this distance (which is the thickness of the new membrane bone), represents the former depth of the excavated fovea. Despite the fact that such dramatic modifications have been made in the aqueduct and the fovea, the layer of endosteal (internal periosteal) bone remains unchanged. Rebuilding of the aqueduct, like that earlier described for the tympanic wall of the lateral semicircular canal, in no manner affects the structure of the layer which, as the innermost of the three osseous laminae, forms the boundary of the labyrinthine (periotic) system of spaces.

On the basis of types of tissue, it may be said that in the fetus of 15 weeks (111 mm.) the capsule is still completely cartilaginous. As ossification centers appear, one of them, in the fetus of 18% weeks (150 mm.), occurs on the cranial aspect of the otic capsule; in this position it makes up part of the medial wall of the vestibule, common crus and semicircular canal, and lines the lateral wall of the cranial aperture of the vestibular aqueduct and of the adjacent fovea for the otic sac.

In the fetus of 21 weeks (183 mm.) bone from several ossification centers has already contributed the three typical layers to the capsule. The periosteal layer is limited to the medial surface of the ledge, or shelf-like projection. The endosteal layer provides an uninterrupted wall for the labyrinth. The middle layer occurs sparsely in the form of cartilage islands, and, peripherally, as a discontinuous layer in which the chondral islands are already imbedded in endochondral bone. In this form, the layer lines the aqueduct and fovea, here being exposed to the meningeal tissue.

In the fetus of 24 weeks (215 mm.) the middle layer is undergoing erosion, especially on the wall of the fovea. The outer layer, on the contrary, confined in this area to the medial (cranial) surface of the ledge, is much thicker than it was in the preceding stage. Production of membrane bone has been initiated on the medial wall of the aqueduct (that is, on the medial wall of the ledge).


In the infant of 10 weeks, membrane bone has filled the foveate excavation; and, in surrounding the otic sac, has formed a new channel for the latter. The periosteal layer is thick; additionally, it has attained petrous nature, as has also the middle layer (in which cartilage islands are still numerous and _ easily distinguishable). During all of these changes, the inner layer remains quiescent.

It is because the ‘“‘adult’’ position of duct and sac is assumed and mature curvature established in the infant, not in the fetus, that remodelling of the aqueduct and fovea must take place in bone, not in cartilage. A very different series of events accompanies, or rather, permits, enlargement of the ares of the semicircular ducts: cartilage is removed peripherally to permit of their advance; new tissue is concurrently produced to maintain the canalicular configuration of the surrounding periotic spaces. This process is aided by a process of dramatically rapid excavation, which swiftly removes the cartilage tissue in the subarcuate fossa.


Thus it is that two neighboring areas of the otic capsule follow markedly different patterns of development. Neither of these schemes of reconstruction is comparable to the excessively slow series of structural changes which takes place, in many specimens, in the region of the fissula ante fenestram. Although the fissula is formed so early that its typical form, contents and parietal layers are established in late fetal life, yet histologic instability seems to characterize the region in postnatal stages. Either within the fissular channel, or in tissues which immediately bound the latter, cartilage and bone retain power of activity —and with such frequency that the region has long been recognized as the site of predilection for the production of the vascular, invasive bone of otosclerosis. These observations lead inescapably to the conclusion that the relatively early attainment of seeming adulthood by tissues of the capsule does not necessarily preclude malleability. The observations further suggest that other factors must be operative in the local production of bone of otosclerotic type.

References

Anson, B. J. and Bast, T. H.: The Development of the Auditory Ossicles and Associated Structures in Man, Ann. Otol., Rhin. & Laryng., 55:467-494, 1946.

Anson, B. J., Cauldwell, E. W. and Bast, T. H.: The Fissula Ante Fenestram of the Human Otic Capsule. I. Developmental and Normal Adult Structure, Ann. Otol., Rhin. & Laryng., 56:957-985, 1947.

Anson, B. J., Cauldwell, E. W.and Bast, T. H.: The Fissula Ante Fenestram of the Human Otic Capsule. II]. Aberrant Form and Contents. Ann. Otol., Rhin. & Laryng., 57:103-128, 1948.

Anson, B. J., Bast, T. H. and Cauldwell, E. W.: The Development of the Auditory Ossicles, the Otic Capsule and the Extracapsular Tissues, Ann. Otol., Rhin., & Laryn., 57:603-632, 1948.

Anson, B. J. and Bast, T. H.: The Development of the Otic Capsule in the Region of Surgical Fenestration, Ann. Otol., Rhin. & Laryng., 58:739-750, 1949.

Bast, T. H. and Anson B. J.: Postnatal Growth and Adult Structure of the Otic (Endolymphatic) Sac, Ann. Otol., Rhin. & Laryng., 59: 1088-1101, 1950.



Cite this page: Hill, M.A. (2024, March 28) Embryology Paper - The development of the otic capsule in the region of the vestibular aqueduct. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_development_of_the_otic_capsule_in_the_region_of_the_vestibular_aqueduct

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