Corticostriatal connectivity in the macaque brain

Abstract

In the macaque brain, projections from distant, interconnected cortical areas converge in specific zones of the striatum. For example, specific zones of the motor putamen are targets of projections from frontal motor, inferior parietal, and ventrolateral prefrontal hand-related areas and thus are integral part of the so-called “lateral grasping network.” The present thesis presents two studies on two aspects of the corticostriatal connectivity in the macaque brain whose results extend current models of corticostriatal interactions. In the study 1, we analyzed the laminar distribution of corticostriatal neurons projecting to different parts of the motor putamen and caudate. After injections of retrograde neural tracers in different parts of the striatum, the laminar distribution of the labeled corticostriatal neurons was analyzed quantitatively. In frontal motor areas, frontal operculum, and prefrontal cortex, where most labeled cells were located, almost everywhere the proportion of corticostriatal labeled neurons in layers III and/ or VI was comparable or even stronger than in layer V. Furthermore, within these regions, the laminar distribution pattern of corticostriatal labeled neurons largely varied independently from their density and from the projecting area/sector, but likely according to the target striatal zone. Accordingly, the present data show that cortical areas may project in different ways to different striatal zones, which can be targets of specific combinations of signals originating from the various cortical layers of the areas of a given network, suggesting more complex modes of information processing in the basal ganglia for different motor and nonmotor functions and opening new questions on the architecture of the corticostriatal circuitry. In the study 2, again based on neural tracer injections in different parts of the striatum, we analyzed and compared qualitatively and quantitatively the distribution of labeled CSt cells in the two hemispheres in macaque brain. The results showed that crossed CSt projections to the caudate and the putamen can be relatively robust (up to 30% of total labeled cells). The origin of the direct and the crossed CSt projections was not symmetrical as the crossed ones originated almost exclusively from motor, prefrontal, and cingulate areas and not from parietal and temporal areas. Furthermore, there were several cases in which the contribution of contralateral areas tended to equal that of the ipsilateral ones. This study is the first detailed description of this anatomic pathway of the macaque brain and provides the substrate for bilateral distribution of motor, motivational, and cognitive signals for reinforcement learning and selection of actions or action sequences, and for learning compensatory motor strategies after cortical stroke.