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Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus)

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DOI: 10.1016/0306-4522(86)90159-4


Abstract The organization of the subcortical connections of caudate nucleus and putamen in the squirrel monkey was studied using horseradish peroxidase conjugated to wheat germ agglutinin as anterograde and retrograde neuronal tracer. The tracer was injected in similar quantities in the putamen on the left side and in the caudate nucleus on the right side in 10 monkeys, and its presence was revealed by means of the tetramethylbenzidine method. The study of anterogradely labeled fibers visualized after such injections shows that putaminofugal fibers terminate massively in the ventral two-thirds of the globus pallidus, where they display a band-like arrangement, and much less abundantly in the caudal third of the substantia nigra. In contrast, caudatofugal fibers occupy only the dorsal third of globus pallidus but arborize profusely in the rostral two-thirds of substantia nigra. In the pars reticulata of the substantia nigra the caudatonigral fibers form a highly complex network composed of fiber trabeculae while the putaminonigral fibers occur as more discrete fascicles confined to the dorsolateral region of the structure. In the pars compacta of the substantia nigra the retrogradely labeled cells occur in the form of clusters that are closely intermingled with clusters of unlabeled neurons. The labeled-cell clusters are particularly dense on the putamen-injected side and more loosely organized on the caudate-injected side. On both sides, however, the striatonigral fibers that reach the substantia nigra pars compacta can be seen to terminate almost exclusively upon clusters composed of retrogradely labeled cells, suggesting the existence of a precise reciprocal link between nigral and striatal neuronal aggregates. At thalamic levels the retrogradely labeled cells are distributed according to a strikingly asymmetric pattern. For instance, a prominent labeling of neurons in the central superior lateral nucleus is seen only on the caudate-injected side. Furthermore, in the centromedian/parafascicular complex retrograde cell labeling is seen exclusively in parafascicular nucleus on the caudate-injected side and only in the centromedian nucleus, except its lateralmost portion, on the putamen-injected side. Control experiments involving injection of the tracer in cerebral cortex overlying the striatum reveal that the neurons in the lateral segment of the centromedian, which do not project to striatum, are in fact reciprocally connected with the cerebral cortex. In addition, our data show that some of the so-called “specific” thalamic nuclei contribute significantly to the thalamostriatal projection in monkey. A particularly prominent projection arises in the ventral anteriorventral lateral nuclei where neurons projecting either to putamen or caudate nucleus occupy different territories. Finally, a significant number of striatal afferent neurons also occurs in midbrain raphe nuclei, pedunculopontine nucleus and amygdala. These various findings indicate that the subcortical connections of caudate nucleus and putamen in primates are organized according to patterns that are markedly different but also largely complementary to one another.

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