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Keywords:

  • vestibular;
  • hair cells;
  • ribbon synapses;
  • efferent synapses;
  • semicircular canals;
  • otolith organs;
  • maculae

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 (Fernández et al. [1995] J. Neurophysiol. 73:1253–1269). To study how this affects 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 (Lysakowski et al. [1995] J. Neurophysiol. 73:1270–1281), reinforcing the importance of inner-face ribbons in synaptic transmission. Comparisons across mammalian species suggest that the prevalence of type I HCs is a primate characteristic, rather than an arboreal life-style 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. J. Comp. Neurol. 511:47–64, 2008. © 2008 Wiley-Liss, Inc.