Basic and Applied Aspects of Vestibular Function

1. The functional organization of the vestibular labyrinth and of some of its central pathways

Basic and AppliedAspects o/Vestibular Function J.C. Hwang, N.G. Daunton and V.J. Wilson (Eds.)© Hong Kong University Press, Hong Kong, 1988 THE FUNCTIONAL ORGANIZATION OF THE VESTIBULAR LABYRINTH AND OF SOME OF ITS CENTRAL PATHWAYS I.M. Goldberg, L.B. Minor and C. Fernandez Department ofPharmacological and Physiological Sciences and ofSurgery (Otolaryngology-Head &Neck Surgery), University ofChicago, Chicago, IL 60637, U.SA. Abstract The relation between the peripheral morphology and the physiology of vestibular -nerve afferents was studied in the semicircular canals of the chinchilla. Some fibers end as calyces supplying type I hair cells. Other fibers give rise to boutons contacting type II hair cells. Still other fibers, so-called dimorphic afferents, innervate both type I and type II hair cells. Dimorphic units make up 70%, bouton units 20%, and calyx units 10% of canal afferents. The three fiber types differ in the diameters of their parent axons and in the regions of the crista they supply. Fiber diameters are largest for calyx fibers and smallest for bouton fibers. Calyx units are confined to the central zone of the crista. Bouton units are restricted to the peripheral zone. Dimporhic units are seen throughout the crista. Two physiological groups of afferents are distinguished on the basis of their discharge regularity and rotational gains. The first group, consisting of dimorphic and bouton units, includes regular, intermediate and high-gain irregular afferents. The second or calyx group are low-gain irregular afferents. The contributions of various afferent contingents to central pathways were studied in the squirrel monkey. Intracellular recordings made from secondary vestibular neurons demonstrate that ipsilateral vestibular-nerve (Vi) inputs remain partially segregated in the vestibular nuclei. Vestibulo-ocular and vestibulospinal neurons receive most of their inputs from regular and irregular afferents, respectively. Flocculus-projecting neurons were particularly heterogeneous in their Vi inputs. A method was devised that results in a selective and reversible ablation of irregular afferents. Functional ablations, done in alert monkeys, show that the vestibulo-ocular reflex receives its predominant input from regular afferents. Keywords: vestibular morphology, vestibular afferent physiology, irregular afferents, regular afferents, secondary vestibular neurons, vestibulo-ocular reflex 4 Goldberg et al. Introduction This paper will consider two topics: (1) the morphological and functional organization of the labyrinthine end organs; and (2) the contributions of various classes of vestibular-nerve afferents to different central pathways. The topics are interrelated. One cannot understand the functional organization of the end organs without understanding how the information provided by them is used by the brain. Similarly, the organization of the central pathways must reflect the organization of their labyrinthine inputs. Attention will be confined to the semicircular canals. Labyrinthine Endorgans Morphological Organization Extracellular horseradish peroxidase (HRP) techniques have been used in the chinchilla to study the peripheral innervation patterns of vestibular afferents (Fernandez et al., in press). Three kinds of terminals can be recognized. Some fibers end as calyces supplying type I hair cells (Fig. Ia & b). Other fibers give rise to boutons contacting type II hair cells (Fig. Id). Still other fibers, so-called dimporphic afferents, innervate both type I and type II hair cells (Fig. Ic). Dimporphic units make up 70%, bouton units 20%, and calyx units 10% of canal afferents. The three fiber types differ in the diameters of their parent axons / b ~~I 1 ~ 1- " d Fig. 1. Reconstructions of two calyx units (a, b), a dimorphic unit (c), and a bouton unit (d), all taken from the horizontal canal crista of a chinchilla. The points at which the parent axons of labelled afferents enter the sensory epithelium are indicated on a standard surface reconstruction. Bar, 1O~m. (From Fernandez et al., in press.) Functional Organization of the Vestibular Labyrinth 5 and in the regions of the crista they supply. Fiber diameters are largest for calyx fibers and smallest for bouton fibers. Calyx units are confined to the central zone of the crista. Bouton units are restricted to the peripheral zone. Dimporhic units are seen throughout the crista. Our classification of afferents is similar to that adopted by Lorente de No (1926). His thick, medium-sized and thin afferents correspond, respectively, to our calyx, dimorphic and bouton fibers. Although the three afferent classes have been previously described, their relative numbers had apparently not been appreciated. The dimorphic units are of particular interest. They are the most numerous type of afferent fiber and are the only units found in all regions of the...