Structural basis for mechanical transduction in the frog vestibular sensory apparatus: III. The organization of the otoconial mass

The saccule and the utricle of the vestibular system detect linear accelera tion and gravity. Sensory transduction in these organs depends on myriads o f calcium carbonate crystals of high specific gravity, called otoconia, emb edded in a filament matrix that overlies the sensory epithelium. The coexis tence of hard crystals and slender filaments in this complex extracellular matrix makes it difficult to analyze by conventional electron microscopy. W e have now examined this structure in the bullfrog saccule using the quick- freeze, deep-etch replica technique. The otoconia in their typical aragonit e polymorph shape exhibit smooth surfaces and are embedded in a loose matri x made of two types of filaments. The regular surface of the otoconia forms a natural smooth background against which we could observe with unpreceden ted detail the network organization and substructure of the filaments. One type of filament is 8 nm in diameter, while the other, which has a characte ristic beaded appearance, is 15 nm in diameter. Both types of filaments eit her make lateral connections with or end directly on the surface of the oto conia. A consistent observation was the presence of short filaments that di rectly cross-link adjacent otoconia. Very few otoconia were fractured in an orientation that would allow the study of their internal architecture. The se otoconia presented a typical conchoidal cleavage of aragonite. Although crystallites were not clearly apparent, thin lamellar microstructures appea red oriented both perpendicularly and longitudinally to the major otoconial axis. This structural study establishes a framework for the identification of the molecular components present in this unique extracellular matrix an d may also help elucidate their role in mechanical transduction. (C) 1999 E lsevier Science B.V. All rights reserved.