Evidence for the coexistence of segregated and integrated functional connections from the striatum to the substantia nigra in rats

The issue of information transfer within the basal ganglia - whether pathways can best be represented by parallel segregated or integrate-and-converge models - is approached. Using manganese enhanced MRI together with a unique principal component analysis method, we present evidence that connectivity from the striatum (the caudomedial part of the caudate putemen (CPu) in rats) to the substantia nigra (SN) is composed of both segregated and integrated projections. Direct intra cranial injection to the rat CPu of paramagnetic manganese ions (MnCl2; 0.2 μl, 0.04 M), which are known to enter neurons, transfer in an anterograde fashion, and cross synapses, was monitored for 72 h by T1-weighted MRI. Signal enhancement was initially seen at the dorsolateral aspect of the SN, and then propagated to the ventromedial part of the nucleus. At 24 h post injection, it started to decline from the periphery to the center. Two principal temporal components were found in all animals. One (PC1; 62% ± 12) was characterized by a moderate ascending slope followed by a slow descent, whereas the other (PC2; 24% ± 7) was characterized by a sharp increase followed by a sharp decrease. Both were localized in the SNr area: PC1 was more disperse, whereas PC2 was smaller and confined to the dorsolateral and medial aspects of the nucleus. We hypothesize that PC2 represents a direct striatum-SN connection while PC1 could represent a striatum-intranigral, an intrastriatal-SN projection, or a third participant. The data support a dynamic organizational view in which the initial segregated pathway is later followed by converging channels.