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. 2018 Aug 2;7(8):bio034462.
doi: 10.1242/bio.034462.

Ectopic Otoconial Formation in the Lagena of the Pigeon Inner Ear

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Free PMC article

Ectopic Otoconial Formation in the Lagena of the Pigeon Inner Ear

E Pascal Malkemper et al. Biol Open. .
Free PMC article

Abstract

The vertebrate inner ear contains vestibular receptors with dense crystals of calcium carbonate, the otoconia. The production and maintenance of otoconia is a delicate process, the perturbation of which can lead to severe vestibular dysfunction in humans. The details of these processes are not well understood. Here, we report the discovery of a new otoconial mass in the lagena of adult pigeons that was present in more than 70% of birds. Based on histological, tomographic and elemental analyses, we conclude that the structure likely represents an ectopically-formed otoconial assembly. Given its frequent natural occurrence, we suggest that the pigeon lagena is a valuable model system for investigating misregulated otoconial formation.This article has an associated First Person interview with the first author of the paper.

Keywords: Avian lagena; Dark cells; Inner ear; Magnetoreception; Otolith; Tegmentum vasculosum; Vestibular organs.

Conflict of interest statement

Competing interestsThe authors declare no competing or financial interests.

Figures

Fig. 1.
Fig. 1.
An otoconial mass (arrowheads) at the dorsal roof of the adult pigeon lagena. (A-I) Stereomicroscope images of lagenae of freshly hatched (A,D,G), 14-18 days old (B,E,H) and over 1-year-old birds (C,F,I). The number in the lower right indicates the animal number and whether the left (L) or right (R) ear is depicted. (J) The new structure was not observed in 1-day-old birds (n=17 ears), rarely in birds aged 14-18 days (19%, n=16 ears) and frequently in adult birds (72%, n=23 ears). (K) The mean diameter of the structure did not differ between young and adult birds. Bars and error bars represent mean±s.d. Scale bar: 500 µm.
Fig. 2.
Fig. 2.
High resolution µCT reconstructions of the pigeon inner ear (n=3 birds, n=6 ears). (A) Reconstruction of the right pigeon bony labyrinth and stapes (St), showing the otoconial masses within the utricle (Ut), saccule (Sa) and lagena (La). (B) Reconstruction of the pigeon lagena showing the position of the second otoconial aggregate above the main horseshoe-shaped otoconial mass. (C) Reconstructions of two lagenar otoconial masses, illustrating their positions relative to each other. Scale bars: 3 mm (A) and 500 µm (C).
Fig. 3.
Fig. 3.
Histological sections reveal that the otoconia are enclosed by an acellular membrane and are not innervated. (A) Light micrograph of the pigeon lagena shown in Fig. 1I, with the plane of sectioning indicated by the dashed line. (B) Paraffin section (10 µm) showing the fine crystal structure and membranous margins of the ectopic otoconia. (C) Immunohistological staining with the postmitotic neuronal marker (TuJ1) (n=3 birds). Staining at the base of lagenar hair cells (HC, black dashed box) was observed, but no signal was observed in the vicinity of the ectopic otoconial mass (OM, white dashed box). (D) Cryo-section (12 µm) showing the ectopic otoconia, magnified in inset. (E) Immunohistological staining with the hair cell marker otoferlin (n=3 birds). The lagenar hair cells (lower right) were stained. (F) Overlay of the unstained and stained section (D,E) illustrating an absence of positive staining in the vicinity of the ectopic otoconia. Scale bars: 100 µm.
Fig. 4.
Fig. 4.
High resolution elemental analysis using synchrotron x-ray fluorescence microscopy demonstrates high calcium and low trace element concentrations within the additional otoconial mass (bird A520, right ear). (A) Light micrograph of the pigeon lagena shown in Fig. 1C, with the plane of sectioning indicated by the dashed line. (B) A 60 µm thick cryo-section dried onto a silicon nitride membrane. (C) X-ray fluorescence spectra of the indicated region of interest with the most prominent peaks assigned to elements. Note the close association with the iron-rich tegmentum vasculosum. (D) X-ray fluorescence maps showing the distribution of iron, potassium, calcium, manganese, zinc, and nickel in the region of the otoconial mass. Arrowheads point to otoconial mass. HCs, hair cells; TV, tegmentum vasculosum. Scale bars: 500 µm (A); 1 mm (B) and 50 µm (C).
Fig. 5.
Fig. 5.
Model showing the additional otoconial mass in the pigeon inner ear lagena. (A) Diagram of the pigeon inner ear, indicating the position of the three otoconia-containing organs: saccule, utricle and lagena. The small dot in the lagena shows the position of the newly-discovered otoconial mass. Sketch based on a reconstruction of the bony labyrinth from µCT scans of a pigeon right ear. (B) Diagram indicating the transitional area between the pigeon basilar papilla and lagena where the additional otoconial mass is located. (C) Diagram of a lagena in the plane indicated by the dashed line in B. The close relationship of the additional otoconial mass to the dorsal tegmentum vasculosum is depicted.

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