The prefrontal cortex (PFC) and insula, amygdala, and striatum form interconnected networks that drive motivated behaviors. We previously found a connectional trend in which granularity of the ventromedial and orbital PFC/insula predicted connections to the amygdala, and also the breadth of amygdalo-striatal efferents, including projections beyond the “classic” ventral striatum. To further interrogate connectional relationships among the cortex, amygdala, and striatum, and to further define the “limbic” (amygdala-recipient) striatum, we conducted tract tracing studies in two cohorts of macaques (male n = 14, female n = 1). We focused on the cortico-amygdalo-striatal (indirect) and cortico-“limbic” striatal (direct) paths originating in the entire PFC and insula. Larger datasets and a quantitative approach revealed “cortical rules” in which cortical granularity predicts the complexity and location of projections to both the basal nucleus of the amygdala and striatum. Remarkably, projections from “cortical-l...