Utricular afferents: morphology of peripheral terminals

Abstract

The utricle provides critical information about spatiotemporal properties of head movement. It comprises multiple subdivisions whose functional roles are poorly understood. We previously identified four subdivisions in turtle utricle, based on hair bundle structure and mechanics, otoconial membrane structure and hair bundle coupling, and immunoreactivity to calcium-binding proteins. Here we ask whether these macular subdivisions are innervated by distinctive populations of afferents to help us understand the role each subdivision plays in signaling head movements. We quantified the morphology of 173 afferents and identified six afferent classes, which differ in structure and macular locus. Calyceal and dimorphic afferents innervate one striolar band. Bouton afferents innervate a second striolar band; they have elongated terminals and the thickest processes and axons of all bouton units. Bouton afferents in lateral (LES) and medial (MES) extrastriolae have small-diameter axons but differ in collecting area, bouton number, and hair cell contacts (LES ϾϾ MES). A fourth, distinctive population of bouton afferents supplies the juxtastriola. These results, combined with our earlier findings on utricular hair cells and the otoconial membrane, suggest the hypotheses that MES and calyceal afferents encode head movement direction with high spatial resolution and that MES afferents are well suited to signal three-dimensional head orientation and striolar afferents to signal head movement onset. hair cells; turtle; utricle; vestibular afferents THE VESTIBULAR LABYRINTH is poorly understood compared, for example, to the auditory periphery and the retina. This is especially true of the major otoconial organs, the utricle and saccule, which encode linear head accelerations, including head position in gravity space, and transmit this information to the CNS. One important question is how the sensory surface of otoconial organs is organized to transduce the full range of signals generated by head movement. There are two broad possibilities: 1) all regions are equipotential in their ability to encode temporal properties of head movement (e.g., different frequencies, accelerations) or 2) different regions of the macula play distinctive functional roles.Considerable evidence supports the second of these alternatives. 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

Specializations for Fast Signaling in the Amniote Vestibular Inner Ear

“…How do the hair cell/synapse categories relate to the epithelial zones? In the utricular epithelia of reptiles (Huwe et al 2015;Jorgensen 1974) and birds (Si et al 2003), the relationship is simple: type I hair cells and their calyceal endings are specific to the striolar zone; type II hair cells and their bouton contacts are found in both zones. In the lagena and saccule of birds, the presence of type I hair cells and calyces has been used to define the striola, producing a zone that is a much broader swath of the epithelium than the striola of avian utricle.…”

Large-Scale Convergence of Receptor Cell Arrays Onto Afferent Terminal Arbors in the Lorenzinian Electroreceptors of Polyodon

“…Bouton endings were visible along the superficial borders of ENs ( Figure 5E). These boutons were comparable to the postsynaptic endings of vestibular afferents onto type II hair cells (Fernández et al, 1995;Huwe et al, 2015).…”

“…For example, usually 10-20 Merkel cells contact an afferent in the light touch mechanoreceptors of mammalian skin (Lesniak et al, 2014). Certain vestibular afferents likely receive synaptic excitation from 5 to >80 hair cells (Huwe et al, 2015). Visceral afferents may show a high degree of convergence and extensive terminal branching arising from a single axon (Spencer et al, 2014).…”

AMPA receptor-mediated rapid EPSCs in vestibular calyx afferents

“…In the striola of the turtle lagena, average spontaneous EPSC activity was reported to be much higher at 52 Hz (Highstein et al 2015). Almost all of our recordings were from isolated calyces containing a single HCI, whereas multicalyces, enveloping up to five HCIs, are frequently found in turtle otolith organs (Highstein et al 2015;Huwe et al 2015). Transmitter release from a greater number of presynaptic ribbons could contribute to the enhanced activity in turtle calyces, but in general recorded EPSC rates are much higher in amphibian auditory and vestibular epithelia (Highstein et al 2015;; Schnee et al 2013) compared with mammals (Glowatzki and Fuchs 2002;Sadeghi et al 2014;Songer and Eatock 2013).…”