Architecture of the Mouse Utricle: Macular Organization and Hair Bundle Heights

Abstract

Hair bundles are critical to mechanotransduction by vestibular hair cells, but quantitative data are lacking on vestibular bundles in mice or other mammals. Here we quantify bundle heights and their variation with macular locus and hair cell type in adult mouse utricular macula. We also determined that macular organization differs from previous reports. The utricle has approximately 3,600 hair cells, half on each side of the line of polarity reversal (LPR). A band of low hair cell density corresponds to a band of calretinin-positive calyces, i.e., the striola. The relation between the LPR and the striola differs from previous reports in two ways. First, the LPR lies lateral to the striola instead of bisecting it. Second, the LPR follows the striolar trajectory anteriorly, but posteriorly it veers from the edge of the striola to reach the posterior margin of the macula. Consequently, more utricular bundles are oriented mediolaterally than previously supposed. Three hair cell classes are distinguished in calretinin-stained material: type II hair cells, type ID hair cells contacting calretinin-negative (dimorphic) afferents, and type IC hair cells contacting calretinin-positive (calyceal) afferents. They differ significantly on most bundle measures. Type II bundles have short stereocilia. Type IC bundles have kinocilia and stereocilia of similar heights, i.e., KS ratios (ratio of kinocilium to stereocilia heights) approximately 1, unlike other receptor classes. In contrast to these class-specific differences, bundles show little regional variation except that KS ratios are lowest in the striola. These low KS ratios suggest that bundle stiffness is greater in the striola than in the extrastriola.

Distinct capacity for differentiation to inner ear cell types by progenitor cells of the cochlea and vestibular organs

“…In addition to the actin-based stereocilia, vestibular hair bundles and immature cochlear hair bundles have a single kinocilium that is microtubule based and contains acetylated α-tubulin (Li et al, 2008;Ogata and Slepecky, 1995). In our differentiated cells, immunoreactivity to acetylated α3 tubulin was rare: only 4% (9/289) of vestibular hair cell-like cells ( Fig.…”

“…Ten percent (8/83) of myosin VIIA-positive cells derived from vestibular progenitors showed oncomodulin-like immunoreactivity, the same as the percentage of HCs in the mature mouse utricular epithelium that are striolar type I HCs (366/3613; Li et al, 2008). The Ca 2+ -binding protein calretinin (calbindin 2) is strongly expressed in immature HCs as well as in mature type II vestibular HCs and cochlear inner HCs (IHCs) (Dechesne et al, 1994;Desai et al, 2005;Li et al, 2008). The calretinin antibody labeled one-third of Atoh1-nGFP + cells (5/15 cells, one experiment) derived from vestibular tissue ( Fig.…”

Ion channels in mammalian vestibular afferents may set regularity of firing

“…1) and many between-zone differences in patterns of hair cells and afferent and efferent innervation are shared across organs (Goldberg, 1991). The central zone of each canal crista resembles in many ways the striola, a swath within each otolith macula that straddles or borders (see Li et al, 2008) a line at which hair bundles reverse orientation. Likewise, the peripheral zones of cristas resemble the extrastriolar zones of maculas (Fig.…”

“…1 shows part of the Firing patterns in vestibular afferents vestibular labyrinth of the mouse inner ear; the utricular macula and two canal cristas have been exposed by removal of the extracellular matrices. Each epithelium comprises several thousand hair cells (Desai et al, 2005a;Desai et al, 2005b;Li et al, 2008) and supporting cells. The hair cells synapse onto the specialized terminals of primary vestibular afferents, as illustrated schematically in Fig.…”

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

“…In mammals, striolar afferents are reported to have higher gains (spikes/s/unit acceleration) than extrastriolar afferents (Lysakowski and Goldberg 2004). If regional differences in the stiffness of turtle utricular hair cells are also present in mammals, as their bundle structures suggest (Li et al 2008), then striolar bundles in mammals may have higher gains (steeper current-displacement curves) than extrastriolar bundles and so may contribute to the higher gains of their postsynaptic afferents. An additional possibility is that stiffer hair bundles in the striola may contribute to the phasic response properties and high-pass filtering of striolar afferents (Eatock and Songer 2011).…”