Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey

The prefrontal cortex is made up of neocortical areas thought to mediate aspects of the temporal and spatial organization of behavior. One of the prime output targets of the prefrontal cortex is the striatum, which is thought to operate in series with the prefrontal cortex in some neural computations. We have analyzed this prefronto-striatal projection in cynomolgus monkeys by combining anterograde neuronal tract tracing methods with neurochemical markers for the striosome and matrix compartments of the striatum. Our results single out two parts of the frontal cortex as projecting densely to the striosome compartment of the striatum: the posterior orbitofrontal/anterior insular cortex and the mediofrontal prelimbic/anterior cingulate cortex. These areas jointly innervated striosomes in the anterior and ventromedial striatum, mainly in the caudate nucleus. Striosomes in the dorsolateral striatum were never labeled. Thus, the anatomical subsystem defined by striosome affiliation includes three cortical and striatal regions that, in humans, have been implicated in obsessive-compulsive disorder. Nearly all of the remaining parts of the prefrontal cortex studied projected preferentially to the matrix compartment. Most of these prefrontal inputs were also patchy, and many of the patches (matrisomes) were selectively paired with nearby striosomes. The highly fractionated organization of prefrontal inputs to striosomes and matrisomes could form a template for computational networks in the striatum that redistribute prefrontal corticostriatal inputs to serve in context-dependent behavioral planning.