The organization of midbrain projections to the striatum in the primate: sensorimotor-related striatum versus ventral striatum

Abstract

In order to examine the organization of nigrostriatal projections in the primate, the retrograde tracers Lucifer Yellow conjugated to dextran amines and horseradish peroxidase conjugated to wheatgerm agglutinin were injected into different regions of the dorsolateral and ventral striatum. Based on the topography of cortical inputs to the striatum, the dorsolateral striatum is associated with the motor system, and the ventral striatum is related to the limbic system. Our results indicate that although midbrain neurons projecting to the ventral and dorsolateral striatum are mostly separate, there are neurons projecting to these different striatal territories that overlap in the medial substantia nigra. The dopaminergic neurons of the ventral mesencephalon can be subdivided into dorsal and ventral tiers that include the cells of the ventral tegmental area, the substantia nigra pars compacta, and the retrorubral area. Neurons projecting to the ventral striatum are found in both the dorsal and ventral tiers. A large number of neurons occupying the medial densocellular zone of the ventral tier are labeled following injections into different regions of the ventral striatum. Neurons projecting to the sensorimotor-related striatum are derived almost exclusively from the ventral tier. Many of these neurons are located very ventrally in the substantia nigra, where clusters of neurons invade the pars reticulata. In addition, labeled neurons are found throughout the mediolateral extent of the densocellular zone of the pars compacta. Notably, neurons are labeled in the medial densocellular zone following injections into the dorsolateral and ventral striatum. Mesencephalic neurons projecting to different striatal territories are distinct in that dorsal tier neurons mainly innervate the ventral striatum, whereas the ventral columns of neurons in the ventral tier innervate the sensorimotor-related striatum. Thus, the dopaminergic regulation of the sensorimotor-related striatum and the ventral striatum may be different. However, a subgroup of dopaminergic neurons in the medial densocellular zone projects to both striatal territories. Such divergent projections may allow the substantia nigra to serve as a link, connecting different striatal territories, via their connections with the substantia nigra.