Steady-state stiffness of utricular hair cells depends on macular location and hair bundle structure

Abstract

Spoon C, Moravec WJ, Rowe MH, Grant JW, Peterson EH. Steady-state stiffness of utricular hair cells depends on macular location and hair bundle structure. J Neurophysiol 106: 2950-2963. First published September 14, 2011 doi:10.1152/jn.00469.2011.-Spatial and temporal properties of head movement are encoded by vestibular hair cells in the inner ear. One of the most striking features of these receptors is the orderly structural variation in their mechanoreceptive hair bundles, but the functional significance of this diversity is poorly understood. We tested the hypothesis that hair bundle structure is a significant contributor to hair bundle mechanics by comparing structure and steady-state stiffness of 73 hair bundles at varying locations on the utricular macula. Our first major finding is that stiffness of utricular hair bundles varies systematically with macular locus. Stiffness values are highest in the striola, near the line of hair bundle polarity reversal, and decline exponentially toward the medial extrastriola. Striolar bundles are significantly more stiff than those in medial (median: 8.9 N/m) and lateral (2.0 N/m) extrastriolae. Within the striola, bundle stiffness is greatest in zone 2 (106.4 N/m), a band of type II hair cells, and significantly less in zone 3 (30.6 N/m), which contains the only type I hair cells in the macula. Bathing bundles in media that break interciliary links produced changes in bundle stiffness with predictable time course and magnitude, suggesting that links were intact in our standard media and contributed normally to bundle stiffness during measurements. Our second major finding is that bundle structure is a significant predictor of steady-state stiffness: the heights of kinocilia and the tallest stereocilia are the most important determinants of bundle stiffness. Our results suggest 1) a functional interpretation of bundle height variability in vertebrate vestibular organs, 2) a role for the striola in detecting onset of head movement, and 3) the hypothesis that differences in bundle stiffness contribute to diversity in afferent response dynamics.

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

“…Striola receptors are predominantly amphora-shaped type I receptors (37) and have short stiff hair bundles (44, 49), apparently loosely attached to the overlying otolithic membrane (38). This fluid motion within the fluid-filled hole in the gel-filament layer of the otolithic membrane produces a drag force on the hair bundle, causing it to deflect.…”

“…Hair cell height and stiffness have been demonstrated to vary across the macula surface (39, 49, 53–55). The cells which do show high-frequency phase locking are from calyx-bearing afferents originating from the striola (21) with shorter stiffer receptor hair cells.…”

Experimental Measurement of Utricle System Dynamic Response to Inertial Stimulus

“…This turtle species will retain their HC stiffness for periods of 5 h or more with exposure to this bHBSS artificial perilymph solution (Spoon et al 2011). This HC bundle stiffness retention time is well beyond any data collection period utilized here, the maximum being 2 h.…”

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

“…In addition, striolar bundles have kinocilia heights that are very close to the thickness of (i.e: they do not protrude into) the CFL. These properties and the "buttressing," described in Spoon et al (2011b) indicate the striola bundles interaction with the OM is strong. Therefore the measured stiffness (41.6 ± 25.4 pN/µm (Grant et al, 2007)) is assumed to fully contribute to the shear resistance of the CFL; that is to say the in-vitro measurement of the physiological stiffness of the hair bundle should be very close to as if it would behave in-vivo (Spoon et al, 2011b).…”

“…Typical methods that characterize bundle stiffness require measurements at the kinocilium tip: Force applied at the tip of kinocilium divided by linear displacement at the tip of kinocilium (Crawford et al, 1985; Flock et al, 1984; Howard et al, 1986; Spoon et al, 2005; Spoon et al, 2011b; Strelioff et al, 1984). These experiments are then modeled with finite elements using Euler-Bernoulli beam theory (Cotton et al, 2004a; Cotton et al, 2004b; Nam et al, 2005; Silber et al, 2004) which includes the mechanics of bundle and the effect of both moments and shear on the displacement and bending (Beer et al, 2006).…”