Hair Bundle Heights in the Utricle: Differences Between Macular Locations and Hair Cell Types

Abstract

Hair bundle structure is a major determinant of bundle mechanics and thus of a hair cell's ability to encode sound and head movement stimuli. Little quantitative information about bundle structure is available for vestibular organs. Here we characterize hair bundle heights in the utricle of a turtle, Trachemys scripta. We visualized bundles from the side using confocal images of utricular slices. We measured kinocilia and stereocilia heights and array length (distance from tall to short end of bundle), and we calculated a KS ratio (kinocilium height/height of the tallest stereocilia) and bundle slope (height fall-off from tall to short end of bundle). To ensure that our measurements reflect in vivo dimensions as closely as possible, we used fixed but undehydrated utricular slices, and we measured heights in three dimensions by tracing kinocilia and stereocilia through adjacent confocal sections. Bundle heights vary significantly with position on the utricular macula and with hair cell type. Type II hair cells are found throughout the macula. We identified four subgroups that differ in bundle structure: zone 1 (lateral extrastriola), striolar zone 2, striolar zone 3, and zone 4 (medial extrastriola). Type I hair cells are confined to striolar zone 3. They have taller stereocilia, longer arrays, lower KS ratios, and steeper slopes than do neighboring (zone 3) type II bundles. Models and experiments suggest that these location- and type-specific differences in bundle heights will yield parallel variations in bundle mechanics. Our data also raise the possibility that differences in bundle structure and mechanics will help explain location- and type-specific differences in the physiological profiles of utricular afferents, which have been reported in frogs and mammals.

The Increased Sensitivity of Irregular Peripheral Canal and Otolith Vestibular Afferents Optimizes their Encoding of Natural Stimuli

“…Previous studies have shown that afferents supplied by type I hair cells tend to be more irregular in their resting discharges (Goldberg and Fernández, 1977;Si et al, 2003;Xue and Peterson, 2006). It has been hypothesized that type I hair cells evolved in amniotes as an adaptation to changes in natural stimulus statistics resulting from (1) the transition from water (i.e., characterized by resistive hydrodynamic forces) to a landbased environment (Eatock and Songer, 2011) and (2) neck elongation in amniotes (Steinacker, 2004).…”

Biomechanics of hair cell kinocilia: experimental measurement of kinocilium shaft stiffness and base rotational stiffness with Euler–Bernoulli and Timoshenko beam analysis

“…From the current data set, we were not able to determine that height. Kinocilia in the turtle utricle can reach heights of >40m (Fontilla and Peterson, 2000;Xue and Peterson, 2006), but because of limitations of our measurement system the tallest kinocilia we could accurately measure was 26m. Measurements were attempted for three kinocilia with heights of ~33m, but the measurements were discarded due to imprecision (s.d.30-50% of the measured value).…”

“…In this configuration, the kinocilium dominates the bundle mechanics. Such hair cells are found in the extrastriola of the turtle utricle (Xue and Peterson, 2006) and are widespread in the otoconial organs of other vertebrates (Lewis et al, 1985). The kinocilium stiffness, which decreases with an increase in the height of an applied force, dictates how much ofdegradation (Flock et al, 1977;Rüsch and Thurm, 1986;Rüsch and Thurm, 1990).…”

Gentamicin is Primarily Localized in Vestibular Type I Hair Cells after Intratympanic Administration

“…The hair bundle structure in type I hair cells differs from that of type II cells. Type I hair cell bundles are taller and have greater numbers of stereocilia that are larger in diameter (Morita et al 1997;Moravec and Peterson 2004;Xue and Peterson 2006). Because each stereocilium is associated with one to two mechanotransduction channels, the greater number of stereocilia on type I hair cells can produce larger transduction current amplitudes (Denk et al 1995).…”