Ultrastructural analysis of the cristae ampullares in the squirrel monkey (Saimiri sciureus)

Abstract

Type I hair cells outnumber type II hair cells (HCs) in squirrel monkey (Saimiri sciureus) cristae by a nearly 3:1 ratio. Associated with this type I HC preponderance, calyx fibers make up a much larger fraction of the afferent innervation than in rodents . To study how this affected synaptic architecture, we used disector methods to estimate various features associated with type I and type II HCs in central (CZ) and peripheral (PZ) zones of monkey cristae. Each type I HC makes, on average, 5-10 ribbon synapses with the inner face of a calyx ending. Inner-face synapses outnumber those on calyx outer faces by a 40:1 ratio. Expressed per afferent, there are, on average, 15 inner-face ribbon synapses, 0.38 outer-face ribbons and 2.6 efferent boutons on calyx-bearing endings. Calyceal invaginations per type I HC range from 19 in CZ to 3 in PZ. For type II HCs, there are many more ribbons and afferent boutons in PZ than in CZ, whereas efferent innervation is relatively uniform throughout the neuroepithelium. Despite outer-face ribbons being more numerous in chinchilla than in squirrel monkey, afferent discharge properties are similar , reinforcing the importance of inner-face ribbons in synaptic transmission. Comparisons across mammalian species suggest the prevalence of type I HCs is a primate characteristic, rather than an arboreal lifestyle adaptation. Unlike cristae, type II HCs predominate in monkey maculae. Differences in hair-cell counts may reflect the stimulus magnitudes handled by semicircular canals and otolith organs. Keywords vestibular; hair cells; ribbon synapses; efferent synapses; semicircular canals; otolith organs; maculae There are two types of hair cells in the vestibular organs of amniotes, including reptiles, birds and mammals (Wersäll and Bagger-Sjöbäck, 1974;Lysakowski, 1996). Type I hair cells contact calyx endings; type II hair cells synapse on bouton endings. Type II hair cells, which are also present in fish (Boyle et al., 1991;Lysakowski, 1996) and amphibia (Honrubia et al., 1989;Lysakowski, 1996), are found throughout the vestibular neuroepithelia in most amniotes. In contrast, type I hair cells have a restricted distribution in * This study was supported by NIH, the National Institute for Deafness and Communication Disorders R01 DC-02521 (AL) and R01 DC-02058 (JMG).Author for Correspondence: Dr. Anna Lysakowski, Department of Anatomy and Cell Biology, University of Illinois at Chicago, 808 S. Wood St., CME 578, M/C 512, Chicago, IL 60612, USA, Telephone: (312) FAX: (312) (Jørgensen, 1974;Schessel et al., 1991;Brichta and Peterson, 1994;Xue and Peterson, 2006) and birds (Jørgensen and Andersen, 1973;Si et al., 2003;Zakir et al., 2003;Haque et al., 2006), being confined to a central zone in the cristae and to the striola in otolith organs. The saccular macula of birds is an exception to this rule as type I hair cells have a broad distribution throughout much of the neuroepithelim (Jørgensen and Andersen, 1973;Zakir et al., 2003).That both kinds of hair cells are important in ...

Utricular afferents: morphology of peripheral terminals

“…Ultrastructural data will be necessary to resolve this and to determine whether, in fact, the spines form synaptic contacts. Interestingly, spines appear to contact hair cells well above the basolateral region where synaptic ribbons are found (Lysakowski and Goldberg 2008;Wersäll 1954;review: Eatock and Lysakowski 2006). Preliminary data using an antibody against CtBP2 as a synaptic ribbon marker suggest that at least some spine-hair cell contacts involve no synaptic ribbons (Peterson EH, unpublished observation).…”

Loss of α-Calcitonin Gene-Related Peptide (αCGRP) Reduces Otolith Activation Timing Dynamics and Impairs Balance

“…In mammals ( Figures 1A,B ), the efferent vestibular system (EVS) begins as hundreds of parent neurons in the dorsal brainstem, which project bilaterally and then branch extensively to make numerous synapses on type II hair cells and afferent terminals including calyces surrounding type I hair cells (Lysakowski et al, 1995; Holt et al, 2006; Lysakowski and Goldberg, 2008). At these synapses, CGRP is commonly colocalized in presynaptic efferent varicosities with choline acetyltransferase (ChAT), the enzyme that catalyzes the synthesis of acetylcholine (ACh), the predominant EVS transmitter (Goldberg, 2000).…”

Histopathologic Changes of the Inner ear in Rhesus Monkeys After Intratympanic Gentamicin Injection and Vestibular Prosthesis Electrode Array Implantation

“…Figure 1 shows representative images of vestibular neuroepithelia under light microscopy with sufficient morphological detail to distinguish between types I and II hair cells (HCs). Consistent with commonly accepted morphologic criteria (Lysakowski and Goldberg 2008;Merchant 1999;Lyford-Pike et al 2007), type I HCs were identified based on their flask shape and halo-like nerve calyx, whereas type II HCs were cylindrical and lacked a clear nerve chalice. To quantitatively evaluate the distribution of HCs in each vestibular end organ, we adopted methodologies developed by Merchant (Merchant 1999) for quantification of vestibular HCs in horizontally sectioned human temporal bones.…”