Inferior olivary nuclear complex of the rat: morphology and comments on the principles of organization within the olivocerebellar system.

This study was undertaken (1) to provide a description of the normal morphology and anatomical interrelationships within the inferior olivary cell groups and (2) to determine the topographical organization of projections from this nuclear complex to the cerebellum. Conventional histological methods and the technique of retrograde transport of horseradish peroxidase (HRP) and WGA-HRP in conjunction with the sensitive chromogen tetramethyl benzidine were used in this series of experiments. In common with that of other animals, the inferior olivary nucleus of the rat consists of three subdivisions: the medial accessory olive (MAO), dorsal accessory olive (DAO), and principal olive (PO). The MAO is made of several subnuclei including a, b, c, and nucleus beta. On the basis of their common connections, the smaller subnuclei, dorsal cap, ventrolateral out-growth, and dorsomedial cell column can be considered as parts of the MAO. The DAO is made of two subdivisions or lamellae–the dorsal and ventral folds-joined together laterally to form a twisted V-shaped structure. The principal olive consists of dorsal and ventral lamellae. A point-to-point projection was determined for four areas of the cerebellum: the anterior lobe, the posterior vermis, the intermediate and the lateral cerebellum. Analysis of the details of the projection system revealed that distinct groups of cells, here referred to as lamellae, project to sagittal zones of the cerebellum. (1) The medial accessory olive appears to be composed of three lamellae: horizontal, vertical, and rostral. The horizontal lamella (elsewhere denoted as groups a and b) projects to a sagittal zone in the vermal anterior lobe. The vertical lamella (groups c, beta, dorsal cap, ventrolateral outgrowth, and dorsomedial cell column) projects to a sagittal zone in the posterior vermis and the flocculus, and the rostral lamella projects to the lateral cerebellum. (2) The dorsal accessory olive is composed of two distinct lamellae which we have previously denoted as the dorsal and ventral folds. The dorsal fold projects to the vermal anterior lobe and receives afferents from the spinal cord, whereas the ventral fold projects to a sagittal zone in the intermediate cerebellum and receives afferents primarily from dorsal column nuclei. (3) The principal olive contains the two familiar lamellae: dorsal and ventral lamellae, each of which projects to a specific sagittal strip in the lateral cerebellum. Each of these lamellae appears to process information from distinct ascending and descending systems. With regard to olivary projections to cerebellar hemispheric lobules, an organization in the form of a banding pattern was discovered. Each band includes the totality of projections to a given cerebellar hemispheric lobule. Large injections of HRP confined within a cerebellar hemispheric lobule, presumably spanning several sagittal zones, were found to label olivary cells in distinct regions of several olivary subnuclei, i.e., lamellae. These groups of labeled cells together form a band that traverses the olivary complex and is oriented perpendicular to the lamellae. Injections in the rostral lobule, e.g., lobulus simplex, labeled a band of cells dorsally within the olive. Injections in the caudal lobules, e.g., paraflocculus, labeled a band ventrally. An overview of the system revealed a global organization in which the olivocerebellar fibers as a whole rotate 90° before terminating in the cerebellar cortex. In this global mapping the rostral olive projects to the lateral hemisphere, whereas the caudal olive projects to the midvermal area. In addition, another dimension of organization has been considered here. The inferior olive can be divided into three functional regions on the basis of their common afferents and efferents. (1) The dorsal accessory olive and caudal medial accessory olive form a somatic sensory zone. (2) The medial area of the MAO is the visual-vestibular zone. (3) The principal olive in conjunction with the rostral MAO is a third zone integrating inputs from higher centers.