A regional ultrastructural analysis of the cellular and synaptic architecture in the chinchilla cristae ampullares

Abstract

The chinchilla crista ampullaris was studied in 10 samples, each containing 32 consecutive ultrathin sections of the entire neuroepithelium. Dissector methods were used to estimate the incidence of various synaptic features, and results were confirmed in completely reconstructed hair cells. There are large regional variations in cellular and synaptic architecture. Type I and type II hair cells are shorter, broader, and less densely packed in the central zone than in the intermediate and peripheral zones. Complex calyx endings are most common centrally. On average, there are 15-20 ribbon synapses and 25-30 calyceal invaginations in each type I hair cell. Synapses and invaginations are most numerous centrally. Central type II hair cells receive considerably fewer afferent boutons than do peripheral type II hair cells, but have similar numbers of ribbon synapses. The numbers are similar because central type II hair cells make more synapses with the outer faces of calyx endings and with individual afferent boutons. Most afferent boutons get one ribbon synapse. Boutons without ribbon synapses were only found peripherally, and boutons getting multiple synapses were most frequent centrally. Throughout the neuroepithelium, there is an average of three to four efferent boutons on each type II hair cell and calyx ending. Reciprocal synapses are rare. Most synaptic ribbons in type I hair cells are spherules; those in type II hair cells can be spherical or elongated and are particularly heterogeneous centrally. Consistent with the proposal that the crista is concentrically organized, the intermediate and peripheral zones are each similar in their cellular and synaptic architecture near the base and near the planum. An especially differentiated subzone may exist in the middle of the central zone.

Efferent Actions in the Chinchilla Vestibular Labyrinth

“…There are efferent endings on calyx and other afferent terminals (Smith and Rasmussen 1968;Iurato et al 1972;Lysakowski 1996;Lysakowski and Goldberg 1997). Recordings from calyx-bearing afferents in turtles reveal that efferent excitation is the result of an EPSP that is blocked by nicotinic antagonists (Holt et al 2003).…”

“…Most afferents in mammals receive afferent inputs from type II hair cells (Fernández et al 1988(Fernández et al , 1990(Fernández et al , 1995. This is obviously the case for bouton and dimorphic afferents, but even the calyx terminals innervating type I hair cells can be contacted on their outer faces by ribbon synapses from type II hair cells (Lysakowski and Goldberg 1997). Type II hair cells receive a conspicuous efferent innervation (Smith and Rasmussen 1968;Wersall and Bagger-Sjöbäck 1974;Lysakowski 1996;Lysakowski and Goldberg 1997).…”

“…In this regard, vestibular organs are not exceptional (Gacek 1960;Gacek and Lyon 1974;Warr 1975;Goldberg and Fernàndez 1980). Efferent fibers synapse on vestibular hair cells and on calyx endings and other afferent processes (Smith and Rasmussen 1968;Iurato et al 1972;Wersäll and Bagger-Sjöbäck 1974;Lysakowski 1996;Lysakowski and Goldberg 1997).…”

“…Among rodents, we chose the chinchilla because extensive studies of the vestibular periphery in this species have provided information about the morphology (Fernández et al 1988(Fernández et al , 1990Lysakowski and Goldberg 1997), physiology Goldberg et al 1990a), and morphophysiology Goldberg et al 1990b) of its afferent innervation and about the morphology of its hair cells (Lysakowski and Goldberg 1997) and of its efferent innervation (Smith and Rasmussen 1968;Marco et al 1993;Ishiyama et al 1994;Bridgeman et al 1996;Lysakowski and Goldberg 1997;Lysakowski and Singer 2000).…”

K+ Currents in Isolated Vestibular Afferent Calyx Terminals

“…Detection of excitatory postsynaptic currents (EPSCs) in solitary gerbil calyces (Rennie and Streeter 2006) and CNQX-sensitive potentials in turtle vestibular afferents support α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-mediated quantal transmission at this synapse (Bonsacquet et al 2006;Holt et al 2007a). Furthermore, in common with other hair cells from the auditory and vestibular systems, there are several ribbon synapses within type I hair cells and their calyces which provide the synaptic machinery for chemical neurotransmission (Lysakowski and Goldberg 1997). However, calyx endings make several invaginations into the type I hair cell where the intercellular cleft narrows to 6-7 nm (Gulley and Bagger-Sjöback 1979).…”