Experimental Measurement of Utricle System Dynamic Response to Inertial Stimulus

Abstract

The membranous utricle sac of the red-eared turtle was mounted in a piezoelectric actuated platform mounted on the stage of a light microscope. The piezoelectric actuator oscillated the base of the neuroepithelium along a linear axis. Displacements were in the plane of the utricle and consisted of a linear sinusoidal-sweep signal starting at 0 and increasing to 500 Hz over 5 s. This inertial stimulus caused measurable shear displacement of the otoconial layer's dorsal surface, resulting in shear deformation of the gelatinous and column filament layers. Displacements of the otoconial layer and a reference point on the neuroepithelium were filmed at 2,000 frames/s with a high-speed video camera during oscillations. Image registration was performed on the video to track displacements with a resolution better than 15 nm. The displacement waveforms were then matched to a linear second-order model of the dynamic system. The model match identified two system mechanical parameters-the natural circular frequency ω n and the damping ratio ζ-that characterized the utricle dynamic response. The median values found for the medial-lateral axis on 20 utricles with 95 % confidence intervals in parenthesis were as follows: ω n = 374 (353, 396)Hz and ζ=0.50 (0.47, 0.53). The anteriorposterior axis values were not significantly different: ω n = 409 (390, 430)Hz and ζ=0.53 (0.48, 0.57). The results have two relevant and significant dynamic system findings: (1) a higher than expected natural frequency and (2) significant under damping. Previous to this study, utricular systems were treated as overdamped and with natural frequencies much lower that measured here. Both of these system performance findings result in excellent utricle time response to acceleration stimuli and a broad frequency bandwidth up to 100 Hz. This study is the first to establish the upper end of this mechanical system frequency response of the utricle in any animal. ρ e -Density of the endolymph; ρ OL -Density of the OL; ω -Excitation frequency; ω n -Undamped natural circular frequency; ζ -Viscous damping factor or damping ratio; γ -Effective shear strain of the SL; τ -Shear stress of the SL acting on the ventral surface of the OL; δ -Deflection of otoconial membrane caused by shear force

Turtle utricle dynamic behavior using a combined anatomically accurate model and experimentally measured hair bundle stiffness

“…Otolithic organs are not seismometers in which the OL displacement would be proportional to earth displacement or a seismic stimulus and would operate above their natural frequency or upper corner frequency. The results shown here support previous claims that turtle utricles, due to their relatively low OL mass, act as accelerometers in the vestibular system with broad frequency bandwidth (Davis et al, 2004; Dunlap et al, 2014; Dunlap et al, 2012; Grant et al, 1986). Afferent recordings from utricles and saccules also support the conclusion that they are accelerometers (Fernandez et al, 1976).…”

“…Any observable increase in stiffness of hair bundles during OM motion would proportionally increase the natural frequency of the OM. However, non-linear behavior was not observed in Dunlap and Grant's (2014) experimental work. We suspect any non-linear effects would be averaged out over the nueroepithelium due to the varied orientations of the bundles and the severity of the non-linear behavior relative to the overall deflection of the OM.…”

“…High natural frequency otolithic organs (mostly utricles) have frequencies in the 350 to 400 Hz range (Dunlap et al, 2014; Dunlap et al, 2012), and low natural frequency otolithic organs (mostly saccules) are in the 20 to 40 Hz range (De Vries, 1951; Narins et al, 1984). The undamped natural frequency of these systems are determined by the square root of the ratio of system stiffness over system mass (see appendix).…”

Sustained and Transient Vestibular Systems: A Physiological Basis for Interpreting Vestibular Function

“…(45, 46). In such models, frequencies in the kilohertz range are beyond the upper mechanical cutoff of the system.…”

Utricular afferents: morphology of peripheral terminals

“…First, the utricle is generally considered to be a dedicated vestibular organ (but see Zhu et al 2014); other otoconial organs such as the saccule and lagena may also function in hearing and seismic detection (Narins and Lewis 1984), which can complicate functional interpretations. Second, more is known about the structure (Moravec and Peterson 2004;Rowe and Peterson 2006;Severinsen et al 2003;Xue et al 2007;Peterson 2003, 2006), physiology (Meyer and Eatock 2011), and mechanical properties (Davis et al 2007; Davis and Grant 2014;Dunlap et al 2012;Dunlap and Grant 2014;Nam et al 2005Nam et al , 2006Nam et al , 2007aNam et al , 2007bSilber et al 2004; of hair bundles and the OM in turtle utricle than in any other species. These data have revealed four structurally and mechanically distinct macular zones (Fig.…”