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The Early Development of the Otic Vesicle in Staged Human Embryos

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The Early Development of the Otic Vesicle in Staged Human Embryos J. Embryol. exp. Morph., Vol. 11, Part 4, pp. 741-755, December 1963 Printed in Great Britain The Early Development of the Otic Vesicle in Staged Human Embryos by RONAN O'RAHILLY1 From the Department of Anatomy, St. Louis University School of Medicine, and the Department of Embryology, Carnegie Institution of Washington WITH TWO PLATES INTRODUCTION EVER since Huschke first recorded, in 1831, that the membranous labyrinth develops from the surface ectoderm (Streeter, 1918), a number of studies of otic development have been made (as reviewed by Altmann, 1950). The introduction during the present century, however, of embryonic staging in all vertebrate classes, and its use especially during the past two decades, have enabled precise correlations of morphogenesis and histogenesis with external embryonic appearances to be made. In the opinion of the present writer, the term 'stage' should not be utilized unless a staging system has been employed, and partic- ularly not where mere time or measurements have been used. Expressions such as 'the 39-day stage' or 'the 18-mm. stage' are thus to be deprecated. In the present study of the otic vesicle, particular attention has been directed to the basement membranes, which have been almost totally ignored in previous accounts both of the developing, and indeed even of the adult, labyrinth. MATERIAL The present account is based on an examination of early, sectioned embryos in the collection of the Department of Embryology, Carnegie Institution of Washington. The planes of section and the stains varied; sixteen of the speci- mens were stained by Mallory's 'azan' procedure. The thirty-six embryos, which extend from stage 9 (3 post-ovulatory weeks) to stage 18 (6 post-ovulatory weeks), are listed in Table 1. The material is classified in stages according to the 'developmental horizons' devised by Streeter. The ages of the embryos can be estimated from their stages, according to the data provided by Olivier & Pineau (1962), as summarized in Table 2. 1 Author's address: Department of Anatomy, Saint Louis University School of Medicine, 1402 South Grand Boulevard, St. Louis 4, Missouri, U.S.A. 742 RONAN O'RAHILLY TABLE 1 Human embryos utilized in the present study of the otic vesicle Stage No. Somites Stage No. Mm. 9 1878 2 13 836 40 10 3709 4 7889 4-2 391 8 9297 4-5 1201 8 8581 4-8 5074 10 8372 5-6 3710 11 14 8308 5-85 3707 12 8999 60 9870 12 6503 6-3 11 7611 16 8552 6-5 470 17 8314 80 5072 17 15 8997 90 8116 17 16 8773 130 12 8943 22 17 8998 110 8505b 23 8789 11 -7 9154 24 18 8355 150 6097 25 9247 150 7852 25 8942 25 5923 28 7724 29 TABLE 2 Approximate length and probable embryonic age of staged human embryos Post-ovulatory Stage Somites Mm. days 9 1-3 20 10 4-12 22 11 13-20 24 12 21-29 26 13 30- 4-6 28 14 5-7 32 15 7-9 33 16 7-11 37 17 11-14 41 18 12-17 44 OBSERVATIONS Stage 9 (1-3 somites) (Plate 1, fig. A) The otic region can first be distinguished in the embryo (No. 1878) of two somites as a thickening on the lateral aspect of the neural fold (Text-fig. 1). It is lined by a basement membrane that is continuous with that of the rhomben- cephalic neural groove. THE OTIC VESICLE IN HUMAN EMBRYOS 743 Comment In an embryo of two or 'possibly three' somites, Wilson (1914) recorded 'a diffuse and rather extensive thickening of the head ectoderm', which 'may possibly foreshadow the appearance of the 'auditory areas'. In the two- somite embryo (No. 1878) referred to above, Ingalls (1920) described a moderate thickening 'about opposite the middle of the rhombencephalon'. He identified it as the 'otic plate' and remarked that its basal surface 'is cleaner and sharper than in the adjacent body-wall and hence more like the neural folds'. The otic TEXT-FIG. 1. Human embryo (No. 1878) of two somites. The left-hand drawing shows the dorsal aspect of the cephalic neural folds; the otic region is shown as a black area on each side. The middle drawing represents the left lateral aspect; the left otic region is indicated in black. The right-hand diagram shows, after median section, the right half of the embryo seen from the medial side. The location of the underlying otic zone is marked by a boundary line on the medial aspect of the right neural fold. zone apparently involves more ectoderm than is eventually incorporated into the otic vesicle. Groth (1939), from his study of the rabbit, preferred to speak of a lateral ridge, or Seitenwulst, from a part {Labyrinthzone) of which the otic plate (Labyrinthplatte) develops. Stage 10 (4-12 somites) (Plate 1, fig. B) The nuclei of the otic plate occupy mostly a basal position, leaving a super- ficial cytoplasmic zone termed the marginal velum. The velum appears to be covered by a terminal bar net (as is the lens at a later stage) and a brush border. Mitotic figures, in this and subsequent stages, are found in the superficial 744 RONAN O'RAHILLY (later central) portion of the plate (as is also the case in the wall of the neural groove and tube). The first indication of invagination of the otic plate is ob- served at ten somites. Neural crest cells, recognizable in this region first at four somites, delaminate from the wall of the neural groove and proceed laterally and ventrally. They are presumed to be the facial, or the so-called acousticofacial, crest. Comment At four somites (No. 3709), Bartelmez (1922) recognized the otic plate and, medial to it, an enlargement in the medial wall of the rhombencephalic neural fold. This swelling was identified as the acousticofaciai division of the neural crest, or the acousticofacial ganglion, which 'arises near, but not exactly at the dorsal edge of the open neural fold' and not 'from cells intermediate between neural and somatic ectoderm'. At eight somites (No. 1201), the otic plate was distinguished by a clear, peri- pheral zone, the marginal velum. As a result of 'the lateral migration of the ganglionic Cells en masse' from the neural fold, an 'otic sulcus' (Bartelmez, 1922) was observed in the ventricular surface of the neural fold. At about nine somites ('Du Ga' embryo), Evans (according to Bartelmez, 1922) noted that the otic plate displayed a peripheral brush border. Moreover, the ganglionic anlage was found to be delaminating from the neural fold. Baxter & Boyd (1938) described an embryo of ten somites in which the 'acousticofacial crest' was continuous across the median plane, an appearance attributed to precocious closure of the neural tube. At twelve somites (No. 8970), invagination of the otic plate was just commenc- ing. The nuclei of the pseudostratified epithelium were basal in position, and PLATE 1 The numeral at the lower right-hand corner of each photograph indicates the embryonic stage. FIG. A. Stage 9. Embryo No. 1878. Section 12-5-7. x270. The otic region constitutes the lateral (right-hand) aspect of the rhombencephalic neural fold. The basement membrane is visible. FIG. B. Stage 10. Alum cochineal. Embryo No. 5074. Section 2-1-2. x270. The nuclei of the otic plate can be seen to occupy mostly a basal position, leaving a marginal velum superficially. FIG. C. Stage 11. Embryo No. 7611. Haematoxylin and eosin. Section 3-19. x270. The otic pit has formed, and appears to be lined by a terminal bar net and a brush border. FIG. D. Stage 12. Embryo No. 9154. Iron haematoxylin and phloxine. Section 2-2-10. x 270. The otic vesicle is forming and its cavity communicates with the surface by a narrow- ing pore. In the lower half of the photograph, the wall of the vesicle appears to be contri- buting to the vestibulocochlear crest. FIG. E. Stage 13. Embryo No. 836. 'Azan.' Section 2-2-3. x200. A projection of the surface ectoderm indicates the site of the connecting stalk which became largely obliterated on closure of the otic pit from the surface. FIG. F. Stage 13. Embryo No. 9297. 'Azan.' Section 3-2-3. x 270. A basement-mem- brane-covered projection of the wall of the otic vesicle constitutes the remains of the con- necting stalk. /. Embryol. exp. Morph. Vol. 11, Part 4 RONAN O'RAHILLY (Facing page 744) THE OTIC VESICLE IN HUMAN EMBRYOS 745 the marginal velum was observed. The mitotic figures were found near the free surface of the plate, that is, adjacent to the brush border. Bartelmez (1922) detected 'a well-developed internal reticular apparatus' in the form of 'a series of clear spaces in the cytoplasm'. Bartelmez & Evans (1926) considered that 'there is some evidence of migration from the otic disc', and it is even possible that the ' seeming spread of the crest cells is really a union of the crest with elements previously proliferated from the ectoderm', including the otic disc. In another twelve-somite embryo (No. 3707) also, an indication of initial invagination of the otic plate was noted. It is now realized that the nuclei of columnar epithelia in vertebrate embryos move temporarily to the free surface before a division. This intermitotic, nuclear migration, which occurs in the neural tube (Sauer & Chittenden, 1959) and its derivatives, in the otic plate and vesicle (Sauer, 1936), and also in the lens plate and vesicle, accounts for the appearance of mitotic figures in a juxta- luminal position. The so-called acousticofacial crest, or the caudate Kopfganglienleiste of Veit, appears to be still the object of considerable controversy.
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