The output organization of the substantia nigra in primate as revealed by a retrograde double labeling method

The cellular origin and degree of collateralization of the efferent projections of the substantia nigra pars reticulata (SNr) in the squirrel monkey (Saimiri sciureus) were studied using the following combinations of fluorescent retrograde tracers: Evans blue and DAPI-Primuline, Fast blue and Nuclear yellow, True blue and Nuclear yellow. In a first series of experiments one tracer was injected in the ventral anterior (VA) and ventral lateral (VL) thalamic nuclei, and the complementary tracer was delivered in the peribrachial area of midbrain tegmentum. After thalamo-tegmental injections numerous nigrothalamic neurons occur in clusters, particularly in rostrolateral part of SNr, whereas the nigrotegmental neurons prevail in caudomedial segment of SNr. However, a significant overlap exists between these two populations. The nigrothalamic and nigrotegmental neurons are present in about equal number in SNr with as much as 60% of these neurons being double-labeled. In a second series of experiments injections were made concomitantly in VA/VL nuclei and in superior colliculus. After thalamo-collicular injections the nigrothalamic neurons are found in larger number than the nigrocollicular neurons which are mostly confined to the middle third of SNr. About 15-20% of all SNr positive neurons are double-labeled, although this proportion climbs to 30-40% in certain sections taken through the middle third of SNr. Finally, injections were made concomittantly in superior colliculus and in midbrain tegmentum. In contrast to the findings obtained after thalamo-tegmental and thalamo-collicular injections, only about 10% of SNr neurons appear to be double-labeled after colliculo-tegmental injections. All injections made in present study have produced retrograde cell labeling in contralateral SNr. However, by far the largest number of contralateral labeled neurons is found after superior colliculus injection. These findings reveal that the SNr neurons in primate, as those in rat and cat, display a high degree of axonal branching. As such, the output organization of SNr appears to differ markedly from that of the substantia nigra pars compacta, but is remarkably similar to that of the internal pallidum which is the other major output structure of the basal ganglia.