Development of otolith receptors in Japanese quail

Abstract

The present study examined the morphological development of the otolith vestibular receptors in quail. Here we describe epithelial growth, hair cell density, stereocilia polarization, and afferent nerve innervation during development. The otolith maculae epithelial areas increased exponentially throughout embryonic development reaching asymptotic values near post-hatch day P7. Increases in hair cell density were dependent upon macular location; striolar hair cells developed first followed by hair cells in extrastriola regions. Stereocilia polarization was initiated early, with defining reversal zones forming at E8. Less than half of all immature hair cells observed had non-polarized internal kinocilia with the remaining exhibiting planar polarity. Immunohistochemistry and neural tracing techniques were employed to examine the shape and location of the striolar regions. Initial innervation of the maculae was by small fibers with terminal growth cones at E6, followed by collateral branches with apparent bouton terminals at E8. Calyceal terminal formation began at E10, however no mature calyces were observed until E12, when all fibers appeared to be dimorphs. Calyx afferents innervating only type I hair cells did not develop until E14. Finally, the topographic organization of afferent macular innervation in the adult quail utricle was quantified. Calyx and dimorph afferents were primarily confined to the striolar regions, while bouton fibers were located in the extrastriola and type II band. Calyx fibers were the least complex, followed by dimorph units. Bouton fibers had large innervation fields, with arborous branches and many terminal boutons.

Morphology and innervation of the vestibular lagena in pigeons

“…Lagenar bouton afferents had the highest terminal density, with nearly four times the number of boutons on average than dimorph fibers. However, lagenar bouton fibers had fewer bouton terminals, than did pigeon utricular or saccular bouton afferents, or even quail utricular fibers (Huss et al, 2010; Si et al, 2003; Zakir et al, 2003). By comparison, pigeon lagenar bouton afferents had an average of 26 bouton terminals, less than that of 60 for the pigeon utricle, 35 for the chinchilla utricle, and 150 for frog utricular fibers (Baird and Schuff, 1994; Fernandez et al, 1990; Si et al, 2003).…”

“…1C). For each hair cell observed in the counting frames, a polarization vector was drawn from the shortest stereocilia to the lone kinocilium through the center of the stereocilia bundle (Huss et al, 2010; Rowe and Peterson, 2004). The vector direction for each cell was quantified, using a compass rosette laid across the epithelium with the form 0° = ventral pole, 90° = posterolateral, 180° = dorsal pole, 270° = anterolateral (Fig.…”

“…However, the otolith organs have received far less attention. Most previous works have concentrated upon the structure of terminal innervations in the utricle, as described for rodents (Desai et al, 2005; Fernández et al, 1990), amphibians (Baird and Lewis 1986, Baird and Schuff, 1994) and birds (Huss et al, 2010; Si et al, 2003). The saccule has only been examined for afferent innervations in fish (Lu and Popper, 2001) and pigeons (Zakir et al, 2003).…”

“…For example, type I hair cells are not present in fish or amphibians (Baird and Schuff, 1994; Chang et al, 1992), but first appear in reptiles and birds (Si et al, 2003; Moravec and Peterson, 2004; Zakir et al, 2003), then reach their highest levels in mammals (Desai et al, 2005; Fernandez et al, 1990). Within birds, the utricle, lagena, and saccule, exhibit increasing numbers of type I hair cells, respectively (Huss et al, 2010; Si et al, 2003; Zakir et al, 2003). …”

“…Calyx afferents had a larger quantity of type I hair cells per fiber, as compared to dimorphs. Birds appear to be unique in having extremely large calyx terminals containing many type I hair cells, both in the semicircular canals and in the otolith maculae (Haque et al, 2006; Huss et al, 2010; Si et al 2003; Zakir et al 2003). However, both the range and the mean number of hair cells/fiber for lagenar calyx afferents were lower than those in pigeon utricular (range 2 – 15, mean of 7.1) and saccular (range 2 – 18, mean of 6.4) afferents.…”