Specializations for Fast Signaling in the Amniote Vestibular Inner Ear

Abstract

During rapid locomotion, the vestibular inner ear provides head-motion signals that stabilize posture, gaze, and heading. Afferent nerve fibers from central and peripheral zones of vestibular sensory epithelia use temporal and rate encoding, respectively, to emphasize different aspects of head motion: central afferents adapt faster to sustained head position and favor higher stimulus frequencies, reflecting specializations at each stage from motion of the accessory structure to spike propagation to the brain. One specialization in amniotes is an unusual nonquantal synaptic mechanism by which type I hair cells transmit to large calyceal terminals of afferent neurons. The reduced synaptic delay of this mechanism may have evolved to serve reliable and fast input to reflex pathways that ensure stable locomotion on land.

Development of hair cell phenotype and calyx nerve terminals in the neonatal mouse utricle

“…Within each epithelium, vestibular hair cells serve as mechanoreceptors for head movements. Mammals have two types of vestibular hair cells—known as Type I and II—that are distinguished by morphological, molecular, and physiological features, as well as by the type of afferent innervation they receive (reviewed in Eatock & Songer, ; Burns & Stone, ; Eatock, ). Type I hair cells are flask‐shaped and have relatively long stereociliary bundles.…”

Efferent Synaptic Transmission at the Vestibular Type II Hair Cell Synapse

“…Each type II HC can form ~ 10-20 ribbon synapses with bouton afferents as well as with the outer wall of calyx terminals (Lysakowski and Goldberg 1997), mediating 'quantal' transmission resulting in glutamatergic EPSPs in afferent endings. Type I HCs transmit signals through quantal EPSPs via ribbon synapses as well as by 'non-quantal' transmission due to accumulation of glutamate, K + , and probably H + in the closed synaptic cleft between type I hair cell and its calyx terminal (Contini et al 2020;Contini et al 2017;Eatock 2018;Highstein et al 2014;Meredith and Rennie 2016;Sadeghi et al 2014;Songer and Eatock 2013). Regarding activation of glutamate release at ribbon synapses, type II hair cells are likely to be more sensitive and respond to smaller stimuli than type I hair cells, due to their ~ 10-fold larger input resistance (Holt et al 1999;Rüsch et al 1998).…”

“…Regarding activation of glutamate release at ribbon synapses, type II hair cells are likely to be more sensitive and respond to smaller stimuli than type I hair cells, due to their ~ 10-fold larger input resistance (Holt et al 1999;Rüsch et al 1998). It has been shown that non-quantal transmission is faster than the glutamatergic quantal transmission (Contini et al 2020;Eatock 2018;Songer and Eatock 2013) and it has been suggested that these two types of HCs likely channel distinct vestibular information to the afferent neurons (reviewed in: Eatock and Songer 2011). As a result, inhibition of type II hair cells by efferents can be a mechanism for decreasing the contribution of bouton terminals and emphasizing the faster dynamics of non-quantal transmission between type I HCcalyx terminals in dimorphic afferents.…”

Cytochrome P450 26b1-mediated specification of vestibular striola and central zones is required for transient responses in linear acceleration

“…Next, we tested whether the VOR was also affected in the Cyp26b1 cKO mutants based on the hypothesis that the striolar/central zone is important for vestibular-reflex function 13,20 . The VOR plays an important role in ensuring gaze stabilization during everyday activities by producing compensatory eye movements in the opposite direction of the head movement 39 .…”

“…Such differences give rise to afferent nerve populations with very different spontaneous and evoked physiological responses. Striolar/central zone afferents have more irregular spike timing and more sensitive to higher-frequency head motion than extrastriolar/peripheral afferents [11][12][13] . Higher densities of low-voltage-activated K (K LV ) channels are expressed in striolar/central zone afferents, making them less excitable -less likely to fire in response to small currents -and more directly driven by synaptic inputs, which contributes to their irregular firing patterns 14 .…”