Autocorrelation Analysis of Hair Bundle Structure in the Utricle

Abstract

The ability of hair bundles to signal head movements and sounds depends significantly on their structure, but a quantitative picture of bundle structure has proved elusive. The problem is acute for vestibular organs because their hair bundles exhibit complex morphologies that vary with endorgan, hair cell type, and epithelial locus. Here we use autocorrelation analysis to quantify stereociliary arrays (the number, spacing, and distribution of stereocilia) on hair cells of the turtle utricle. Our first goal was to characterize zonal variation across the macula, from medial extrastriola, through striola, to lateral extrastriola. This is important because it may help explain zonal variation in response dynamics of utricular hair cells and afferents. We also use known differences in type I and II bundles to estimate array characteristics of these two hair cell types. Our second goal was to quantify variation in array orientation at single macular loci and use this to estimate directional tuning in utricular afferents. Our major findings are that, of the features measured, array width is the most distinctive feature of striolar bundles, and within the striola there are significant, negatively correlated gradients in stereocilia number and spacing that parallel gradients in bundle heights. Together with previous results on stereocilia number and bundle heights, our results support the hypothesis that striolar hair cells are specialized to signal high-frequency/acceleration head movements. Finally, there is substantial variation in bundle orientation at single macular loci that may help explain why utricular afferents respond to stimuli orthogonal to their preferred directions.

Utricular afferents: morphology of peripheral terminals

“…There is also evidence for further macular differentiation beyond the striola: extrastriola dichotomy, including subdivisions within the striola (well documented in nonmammalian amniotes ;Jorgensen 1989;Si et al 2003;Xue and Peterson 2006), differences between the medial (MES) and lateral (LES) extrastriolae (Baird and Schuff 1994;Li et al 2008;Rowe and Peterson 2006;Xue and Peterson 2006), and a possible juxtastriolar region between the striola and the MES (Chang et al 1992;Baird and Schuff 1994;Fernandez et al 1990;Goldberg et al 1990b;Saidel and Crowder 1997). Thus the available data indicate that otoconial maculae may comprise multiple regions with distinctive properties.…”

“…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.…”

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

“…Zone 4 corresponds to the MES. At the lateral edge of zone 4, near its border with the calyx band (zone 3), hair bundle structure changes gradually from a striola-like to an MES-like configuration (Rowe and Peterson 2006;Xue and Peterson 2006); we refer to this band as the juxtastriola. A medial-to-lateral transect (Fig.…”

“…We measured the stiffness of 73 bundles (21 utricles) along this medial-to-lateral transect, concentrating on the striola and adjacent extrastriolae because hair bundle structure is markedly heterogeneous in this region (it is nearly constant in the remainder of the LES and MES; Rowe and Peterson 2006;Xue and Peterson 2006). Thus stiffness measurements within this region are most likely to reveal any dependence of bundle stiffness on bundle structure.…”

“…In this study, we took advantage of the orderly variation in hair bundle structure across the turtle macula (Fontilla and Peterson 2000;Jorgensen 1974Jorgensen , 1988Moravec and Peterson 2004;Rowe and Peterson 2006;Severinsen et al 2003;Xue and Peterson 2006) to examine covariation of bundle structure and stiffness. We had two goals.…”