Abstract

We explored the functional role of individual otoconia within the otolith system of mammalians responsible for the detection of linear accelerations and head tilts in relation to the gravity vector. Details of the inner structure and the shape of intact human and artificial otoconia were studied using environmental scanning electron microscopy (ESEM), including decalcification by ethylenediaminetetraacetic acid (EDTA) to discriminate local calcium carbonate density. Considerable differences between the rhombohedral faces of human and artificial otoconia already indicate that the inner architecture of otoconia is not consistent with the point group -3m. This is clearly confirmed by decalcified otoconia specimen which are characterized by a non-centrosymmetric volume distribution of the compact 3+3 branches. This structural evidence for asymmetric mass distribution was further supported by light microscopy in combination with a high speed camera showing the movement of single otoconia specimen (artificial specimen) under gravitational influence within a viscous medium (artificial endolymph). Moreover, the response of otoconia to linear acceleration forces was investigated by particle dynamics simulations. Both, time-resolved microscopy and computer simulations of otoconia acceleration show that the dislocation of otoconia include significant rotational movement stemming from density asymmetry. Based on these findings, we suggest an otolith membrane expansion/stiffening mechanism for enhanced response to linear acceleration transmitted to the vestibular hair cells.

Highlights

  • The mammalian inner ear realizes its function by means of the mechanical activation of vestibular and auditory hair cells

  • environmental scanning electron microscopy (ESEM) investigations of human and biomimetic otoconia revealed that non-centrosymmetric mass distribution is the predominant feature (Figs 2–5)

  • The behavior of the otoconia resembles that of a buoy (Fig 7)

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Summary

Introduction

The mammalian inner ear realizes its function by means of the mechanical activation of vestibular and auditory hair cells. Utricle and saccule each contain thousands of otoconia embedded in an acellular organic matrix (otoconial complex) [1,2]. Mammalian otoconia with characteristic shape (Fig 1) are arranged to form various layers [5]. Their mean size is about 10 μm, there is a specific size distribution of otoconia over the otolithic membrane, which, is not in the focus of the present investigation [6]. These proteins, such as otoconin 90 and otolin are integrated into the composite structure of otoconia and grow out of otoconial volume to form fibrils, which interconnect otoconia within a flexible network [3,9,10,11]

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