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

doi:10.1016/S0306-4522(98)00681-2

Neuroscience

Volume 91, Issue 3, July 1999, Pages 891-909

https://doi.org/10.1016/S0306-4522(98)00681-2 Get rights and content

Abstract

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.

Section snippets

Animals

Male Sprague–Dawley rats (Charles River, France) were used in all experiments. All efforts were made to reduce the number of animals used and to minimize animal suffering, in compliance with the French décret no. 87 848 dated 19 October 1987 and 19 April 1988.

Application of tracer

The protocol used has been described in a previous report.¹⁰ Briefly, the rats were anaesthetized with ketamine (Imalgene, Rhone-Merieux)–pentobarbital (Sanofi, France) and the WGA–HRP conjugate (2.5% in 0.9% saline) was injected into

Results

The anterograde and retrograde labelling observed in the SN and the cerebral cortex following injections performed in eight striatal functional territories was examined. The striatal injection sites corresponded to the projection zones of the somatic sensorimotor, the visual and auditory sensorimotor and the limbic/prefrontal cortical areas. The volumes of the injection sites and of the anterogradely labelled striatonigral terminal fields, as well as the number of retrogradely labelled nigral

Discussion

Previous studies carried out in our laboratory8., 10. have provided evidence for the existence of a rigorous functional compartmentation of the rat striatonigral circuits. This compartmentation, which globally maintains the major functional subdivisions of the cerebral cortex, results from the anatomical segregation of cortical information within the striatonigral pathways. These studies, which were focused on the descending flow of information from the striatum to the nigrothalamic and

Conclusions

Our results indicate that nigrostriatal neurons are spatially organized so as to respond to the compartmentation of the corticobasal ganglia–thalamocortical circuits into functional channels of information processing. As suggested by the functional organization scheme presented in Fig. 8, the co-existence, for each functional striatal region, of (at least) two spatially distinct subpopulations of nigral neurons may account for various modalities of nigral regulation of striatal activity.

Acknowledgements

We wish to express our thanks to Philippe Nguyen Van Tam (Centre de Traitement et de Production d'Images, UFR des Sciences de la Vie, Université Pierre et Marie Curie, Paris 6) for expert assistance in the realization of the iconographical illustrations.