The sense of balance in humans: Structural features of otoconia and their response to linear acceleration

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.

Semicircular canal biomechanics in health and disease

“…Although often idiopathic, there are identified risk factors for BPPV including vitamin D deficiency, low bone mineral density, and head trauma (Akin et al 2017; Chan et al 2017; Gokler et al 2018; Rhim 2016; Yang et al 2018; Yu et al 2014). Otoconia range in size from less than 1 to 30 µm and are almost threefold denser than endolymph with a specific gravity of ~2.7, (Kniep et al 2017; Lim 1984; Vibert et al 2008). Canalith particles can be free to move within the endolymph causing the condition canalithiasis or can be adhered to the cupula causing the condition cupulolithiasis (Brandt and Steddin 1993; Epley 1992; Hall et al 1979; Parnes and McClure 1992; Schuknecht 1962).…”

Electric-Contact Tilt Sensors: A Review

“…Even more startling is a similarity between this sense and some of mechanical tilt sensors presented later in the text, using a free member for generation of electric-contact between the sensing electrodes and featuring full detection range. External receptors of the human sense of balance consist not only of the semicircular canals but also of the otolith system, which includes the utricle and the saccule [ 2 ], and is located next to the semicircular canals and contains numerous otoliths (crystals of calcium carbonate). The otoliths can freely move while the human accelerates or tilts its head, and thus represent linear motion sensors [ 2 ].…”

“…External receptors of the human sense of balance consist not only of the semicircular canals but also of the otolith system, which includes the utricle and the saccule [ 2 ], and is located next to the semicircular canals and contains numerous otoliths (crystals of calcium carbonate). The otoliths can freely move while the human accelerates or tilts its head, and thus represent linear motion sensors [ 2 ]. Even though the otoliths do not generate an electric contact, as the discussed tilt sensors, they stimulate appropriate receptor cells while relocated or accelerated.…”

Functional derivatives of human dentin matrix protein 1 modulate morphology of calcium carbonate crystals

“…Linear acceleration causes the otoconia, which are denser than the surrounding endolymph, to move relatively to hair cells. This creates a signal, which together with visual stimuli from the eyes is interpreted as a movement . In contrast to bones, which are continuously resorbed and synthesized throughout life, otoconia are formed during the embryonic development, mature during the perinatal period, and do not regenerate later in life.…”