Vestibular Hair Cells and Afferents: Two Channels for Head Motion Signals

Abstract

Vestibular epithelia of the inner ear detect head motions over a wide range of amplitudes and frequencies. In mammals, afferent nerve fibers from central and peripheral zones of vestibular epithelia form distinct populations with different response dynamics and spike timing. Central-zone afferents are large, fast conduits for phasic signals encoded in irregular spike trains. The finer afferents from peripheral zones conduct more slowly and encode more tonic, linear signals in highly regular spike trains. The hair cells are also of two types, I and II, but the two types do not correspond directly to the two afferent populations. Zonal differences in afferent response dynamics may arise at multiple stages, including mechanoelectrical transduction, voltage-gated channels in hair cells and afferents, afferent transmission at calyceal and bouton synapses, and spike generation in regular and irregular afferents. In contrast, zonal differences in spike timing may depend more simply on the selective expression of low-voltage-activated ion channels by irregular afferents.

Coding of envelopes by correlated but not single-neuron activity requires neural variability

“…Interestingly, hair cells giving rise to vestibular afferents with high resting discharge variability can only be found in amniotes. It is, furthermore, thought that their recent evolution was triggered by changes in vestibular stimulus statistics resulting from transitioning from an aquatic to a terrestrial environment (37), which is incompatible with the above point of view that variability is detrimental to neural coding. Alternatively, it has been more recently postulated that neural variability instead forms a key element of the neural code by promoting increased information transmission (1).…”

Hyperpolarization-Activated Current (I h) in Vestibular Calyx Terminals: Characterization and Role in Shaping Postsynaptic Events

“…Firing pattern is either regular or irregular and corresponds to zonal differences in peripheral innervation (Baird et al 1988;Goldberg 2000). Regularly firing afferents terminate in peripheral zones of vestibular sensory epithelia and irregularly firing afferents in more central zones (Goldberg 2000;Eatock and Songer 2011). Intrinsic membrane properties of afferent neurons may play an important role in determining firing pattern and ionic currents described in vestibular ganglion somata include voltage-and calcium-dependent K + currents (Chabbert et al 2001a;Limón et al 2005;Risner and Holt 2006;Iwasaki et al 2008;Kalluri et al 2010), sodium (Chabbert et al 1997) and calcium currents Chambard et al 1999;Autret et al 2005), and a mixed cation hyperpolarization-activated current (I h ) (Chabbert et al 2001b).…”

Utricular afferents: morphology of peripheral terminals

“…The best-known example of regional specializations in otoconial maculae is the ubiquitous division between striola and extrastriola: the striolar region of vertebrate maculae differs from the extrastriola in the structure and molecular composition of the otoconial membrane (OM) (e.g., Goodyear et al 1994;Lim 1979;Lindeman 1969;Werner 1933;reviewed in Fermin et al 1998;Lewis et al 1985), which transmits the mechanical stimuli arising from head movements to receptors (hair cells), and in the structure and physiology of its hair cells (e.g., Baird 1994aBaird , 1994bGoodyear and Richardson 1992;Li et al 2008;Schweizer et al 2009;Weng and Correia 1999; reviews in Eatock and Lysakowski 2006;Eatock and Songer 2011;Lewis et al 1985;Platt 1983) and their postsynaptic primary afferents (e.g., Baird and Lewis 1986;Baird and Schuff 1994;Desai et al 2005;Fernandez et al 1990;Si et al 2003; reviews in Eatock and Songer 2011;Lysakowski and Goldberg 2004). For example, there are three broad classes of primary afferents in amniotes: all-calyx afferents (C units), which contact type I hair cells exclusively; bouton afferents (B units), which contact only type II hair cells; and dimorphic afferents (D units), which contact both hair cell types.…”