Three-dimensional distribution of nigrostriatal neurons in the rat: relation to the topography of striatonigral projections.

Functional regions of the rat striatum related to identified cortical territories were injected ionophoretically with wheat germ agglutinin coupled to horseradish peroxidase. Coronal serial sections were cut throughout the substantia nigra. The distributions of labelled striatal projections and nigrostriatal neurons were studied. Using software developed in our laboratory, three-dimensional reconstructions were calculated which confirmed and extended the organizational scheme of striatonigral projections already reported by our group. These projections were organized as a set of longitudinal lamellae spatially organized so as to segregate the flow of information emanating from striatal regions affiliated to sensorimotor and associative-limbic cortical areas. In addition, the relationship between the striatonigral projections and the nigrostriatal neurons was studied by three-dimensional reconstruction. For each striatal injection site, two populations of retrogradely labelled nigral neurons could be discriminated by their position with respect to the striatal projection field. The first one occupied a proximal position, in register with the labelled striatal projections, while the second was more distal. The populations of proximal neurons which innervate different functional striatal sectors were segregated both mediolaterally, dorsoventrally and rostrocaudally, while the populations of distal neurons were more scattered and showed a lesser degree of spatial segregation. The organization of these two populations with respect to the striatal projection fields suggests that the substantia nigra might control the flow of cortical information through the striatum via two different modalities, based respectively on a closed nigrostriatal loop involving the proximal neurons, and an open loop involving the distal ones.