The primate neocortex is characterized by a highly expanded supragranular layer (SGL). The interareal connectivity of the neurons in the SLG largely determines the cortical hierarchy that constrains information flow through the cortex. Interareal connectivity is made by precise numbers of connections, raising the possibility that the physiology of a target area is dictated by the numbers of connections and hierarchical distance in each of the pathways that it receives. The developmental mechanisms ensuring the precision of these interareal networks is in part determined by (i) the numbers of SGL neurons generated by the OSVZ, a primate-specific germinal zone. Neuron generation rate in the OSVZ is determined by regulation of the G1 phase of the cell-cycle. This regulation is area-specific and is linked to thalamic projections to the OSVZ; (ii) Prolonged pre- and postnatal pruning of connections originating from the SGL when the infant monkey visually explores its environment. Remodelling serves to sharpen initial patterns of connections and establishes the adult hierarchy. These results suggest that primate cortical networks underlying high-level function undergo prolonged self-organization via regressive phenomena in the cortical plate (axon elimination) and progressive phenomena (directed growth of cortical axons).