The lamellar organization of the rat substantia nigra pars reticulata: segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections.

The striatonigral pathway provides one of the most direct routes for information flow through the basal ganglia system. Via this pathway information from sensory, motor and associative areas of the cerebral cortex are routed to a variety of thalamocortical and brainstem networks involved in the organization of motor behaviour. In a previous analysis of the rat substantia nigra pars reticulata we have shown that the nigral cells which project to thalamus, tectum and tegmentum are topographically ordered along a series of curved laminae. Extending these observations, the present study examined how striatal regions related to particular areas of the cerebral cortex innervate the lamellar keyboard of nigral output neurons. For this purpose, small microiontophoretic injections of wheat germ agglutinin conjugated to horseradish peroxidase were performed in the striatum and the distribution of retrogradely-labelled cells in the cerebral cortex and anterogradely-labelled axons in the substantia nigra were conjointly examined. The results indicate that with the exception of the striatal region related to the allocortex, all the various components of the striatal functional mosaic are represented in the substantia nigra pars reticulata. This representation is organized under the form of longitudinal bands which compose a series of curved laminae enveloping a core located dorsolaterally in the substantia nigra. The striatal mapping in substantia nigra pars reticulata is such that the projections of the auditory and visual compartments are confined to the most ventral lamina. More dorsally, an ordered representation of the body is achieved by the nigral lamination. The oral and perioral body parts are centred on the dorsolateral core and the more distal parts of the face and limbs are progressively set out in more peripheral laminae. In the region affiliated to the prefrontal cortex, the dorsal cingulate district innervate a ventromedial lamina, the prelimbic/insular district lie dorsal to it. Projections from lateral orbital and insular compartments extend laterally along the dorsal margin of the pars reticulata. Since the "onion-like" distribution of striatal inputs is precisely the form observed in the distribution of nigral efferent neurons, the present observations favour the view that the nigral lamination underlies formation of specific input-output channels of processing. Evidence is considered that these channels are specialized for particular classes of movements or behaviours and integrate the various information relevant to the completion of these movements or behaviours.