Developmental Morphology of the Mouse Inner Ear: A scanning electron microscopic observation

Abstract

The developing inner ears of mice (CBA/CBA), ages ranging from gestational day 12 through postnatal day 21, were examined using scanning electron microscopy following the epoxy-embedding/freeze-fracture technique. This technique provides unique three-dimensional views of surface and fractured structures of the developing inner ear, thus allowing excellent preservation of the relationships between the developing sensory epithelium and the overlying membranes (i.e. the tectorial membrane and cupula) during their development.The tectorial membrane is formed of two distinct parts: the major (medial) and the minor (distal). The major portion is produced by the cells of the greater epithelial ridge prior to the formation of the minor part, which is produced largely by the primordial supporting cells of the lesser epithelial ridge. The developing tectorial membrane has two types of fibers: radial (found mainly in the major part) and slanted (found mainly in the minor part). The slanted fibers become the cover net, which fuses with the marginal band. The marginal zone of the developing tectorial membrane is completely sealed during development by the third row of Deiters' cells. The surfaces of cells that produce the tectorial membrane are characterized by numerous long microvilli which are largely lost when the tectorial membrane completely forms and separates from the supporting cells.The surface of developing auditory sensory cells is initially covered with numerous microvilli, some of which become future stereocilia. Stereocilia form stepped rows in the shape of a “W”, with the tallest row located at the periphery of the cell. As the sensory cell matures, the short transitional stereocilia gradually disappear. Kinocilia on hair cells are still seen in the 14-day-old mouse (even though the organ of Corti is morphologically mature) but not in the 21-day-old mouse, indicating that complete maturation of the sensory cells in all turns is attained by 21 days of age. The mouse has upper radial tunnel fibers and basal tunnel fibers. Neural contacts of the upper radial tunnel fibers with the outer hair cells at the apical portions are frequent in the developing organ of Corti.The external sulcus cells undergo drastic changes during development, forming numerous pits that are often covered with mucus-like droplets or grape-like spherical structures of varying sizes. This phenomenon was observed only during postnatal days 6 and 14.The developing cupula starts as a thin amorphous membrane, which later becomes compact and fibrotic-like as the mass increases. By the 6th postnatal day well-developed cupular canals occur. In some canals in the central zone of the crista, the tall stereociliary bundles are in contact with a part of the canal wall, but short stereociliary bundles are free-standing in the subcupular space. In the periphery of the crista, the cupular canals are smaller in diameter or are not seen at all at the extreme periphery. Consequently, only the tall ciliary bundles are directly in contact with the cupula.The onset of the development of sensory cilia occurs in the central part of the maculae whereafter the surface differentiation of future hair cells extends towards the periphery. During final differentiation, however, new sensory cells develop in all parts of the sensory epithelium including the central region. The centripetal developmental pattern of vestibular organs was not clearly established in some cristae of the posterior canal. As in the auditory sensory cells, the vestibular sensory hairs develop as a regularization of microvilli covering the future hair cell. Some of these microvilli become short transitional stereocilia, which initially number around 200 but only about 60 develop into fully mature stereocilia having an organ-pipe arrangement. In general, the tall stereocilia develop close to the kinocilium. In rare cases the kinocilium is found in the center of the growing stereocilia. The vestibular sensory epithelia have mature configuration by 6–14 days postnatally.