JOURNAL OF NBUROPHYSIOLOGY Vol. 73, No. 3, March 1995. Printed in U.S.A. Hair-Cell Counts and Mferent I ervation Patterns in the Cristae Ampullares of the Squirrel Monkey With a Comparison to the Chinchilla C&AR FERNANDEZ, ANNA LYSAKOWSKI, AND JAY M. GOLDBERG Departments of Surgery (Qtolaryngology-Head and Neck Surgery) and oj’ Pharmacological and Physiological Sciences, University of Chicago, Chicago, Illinois 60637 SUMMARY AND CONCLUSIONS 1. The numbers of type I and type II hair cells were estimated by dissector techniques applied to semithin, stained sections of the horizontal, superior, and posterior cristae in the squirrel monkey and the chinchilla. 2. The crista in each species was divided into concentrically arranged central, intermediate, and peripheral zones of equal areas. The three zones can be distinguished by the sizes of individual hair cells and calyx endings, by the density of hair cells, and by the relative frequency of calyx endings innervating single or multi- ple type I hair cells. 3. In the monkey crista, type I hair cells outnumber type II hair cells by a ratio of almost 3: 1. The ratio decreases from 4-51 in the central and intermediate zones to under 2:1 in the peripheral zone. For the chinchilla, the ratio is near 1: 1 for the entire crista and decreases only slightly between the central and peripheral zones. 4. Nerve fibers supplying the cristae in the squirrel monkey were labeled by extracellular injections of horseradish peroxidase (HRP) into the vestibular nerve. Peripheral terminations of individ- ual fibers were reconstructed and related to the zones of the cristae they innervated and to the sizes of their parent axons. Results were similar for the horizontal, superior, and posterior cristae. 5. Axons seldom bifurcate below the neuroepithelium. Most fibers begin branching shortly after crossing the basement mem- brane. Their terminal arbors are compact, usually extending no more than SO- 100 pm from the parent axon. A small number of long intraepithelial fibers enter the intermediate and peripheral zones of the cristae near its base, then run unbranched for long distances through the neuroepithelium to reach the central zone. 6. There are three classes of afferent fibers innervating the mon- key crista. Calyx fibers terminate exclusively on type I hair cells, and bouton fibers end only on type II hair cells. Dimorphic fibers provide a mixed innervation, including calyx endings to type I hair cells and bouton endings to type II hair cells. Long intraepithelial fibers are calyx and dimorphic units, whose terminal fields are similar to those of other fibers. The central zone is innervated by calyx and dimorphic fibers; the peripheral zone, by bouton and dimorphic fibers; and the intermediate zone, by all three kinds of fibers. Internal (axon) diameters are largest for calyx fibers and smallest for bouton fibers. Of the entire sample of 286 labeled fibers, 52% were dimorphic units, 40% were calyx units, and 8% were bouton units. 7. Most calyx units in the monkey are unbranched, giving rise to a single calyx ending that innervates one to three adjacent type I hair cells. The terminal arbors of bouton fibers consist of fine collaterals that extend for 30- 100 pm from the parent axon and contain 15-70 endings. Dimorphic fibers have thick branches ter- minating as calyx endings and fine collaterals with bouton endings. Individual dimorphs have l-4 calyx endings and from 1 to > 100 bouton endings; those supplying the central zone have larger axons and simpler trees than those terminating in the peripheral zone. 8. Afferent branching patterns in the monkey cristae were com- pared with those previously described in the chinchilla cristae. Long intraepithelial fibers were seen in the monkey, but not in the chinchilla. In other respects, the afferent innervation is qualitatively similar in the two species. There are quantitative differences in the proportions of calyx, dimorphic, and bouton fibers, in the number of bouton endings provided by dimorphic fibers and in the number of type I hair cells contacted by calyx and dimorphic fibers. The differences serve to match the afferent innervation to the comple- ment of hair cells found in each species. Most of OUI r knowledge of the structure of the mammalian vestibular labyrinth hascome from rodents. This is so for afferent branching patterns (Fernandez et al. 1988, 1990; Lorente de No 1926; Poljak 1927)) synaptic ultrastructure (Wersall 1956; Wersall and Bagger-Sjoback 1974)) and the relation between the morphology of an afferent and its physi- ological properties (Baird et al. 1988; Goldberg et al. 199Oa). Anatomic studies in monkeys have been confined to measurements of the dimensions of the end organs (Igarashi 1967)) to counts of the number of hair cells (lgarashi et al. 1975) , to an analysis of the numbers and sizes of nerve fibers (Fermin and Igarashi 1987; Honrubia et al. 1987), and to an ultrastructural study of the otolith organs (Engstrom et al. 1972). The situation is unfortunate because it would be of interest organs in to compare th e structural organization of the end a variety of mammal % including primates and rodents. In addition, monkeys are becoming increasingly popular choices for the study of central vestibular pathways (see, for example, Fuchs and Kimm 1975; McCrea et al. 1987; Minor and Goldberg 199 1). Interpretation of the cen- tral studies would be helped by a knowledge of the structure and function of the labyrinth in these animals. A goal of this study was to describe the afferent innerva- tion patterns in the squirrel monkey cristae. We were particu- larly interested in comparing results with those previously obtained in the chinchilla (Fernandez et al. 1988). In the latter animal, it was found that afferents innervating each crista could be divided into three classes. Calyx units are thick fibers seen almost exclusively in the central zone of 0022-3077/95 $3.00 Copyright 0 1995 The American Physiological Society 1253