Somesthesis-guided exploration of the external world requires cortical processing of both cutaneous and proprioceptive information and their integration into motor commands to guide further haptic movement. In the past, attention has been given mostly to the cortical circuits processing cutaneous information for somatic motor integration. By comparison, little has been examined about how cortical circuits are organized for higher order proprioceptive processing. Using the rat cortex as a model, we characterized the intrinsic and corticocortical circuits arising in the major proprioceptive region of the primary somatosensory cortex (SI) that is conventionally referred to as the dysgranular zone (DSZ). We made small injections of biotinylated dextran amine (BDA) as an anterograde tracer in various parts of the DSZ, revealing three distinct principles of its cortical circuit organization. First, its intrinsic circuits extend mainly along the major axis of DSZ to organize multiple patches of interconnections. Second, the central and peripheral regions of DSZ produce differential patterns of intra-areal and corticocortical circuits. Third, the projection fields of DSZ encompass only selective regions of the second somatic (SII), posterior parietal (PPC), and primary motor (MI) cortices. These projection fields are at least partially separated from those of SI cutaneous areas. We hypothesize, based on these observations, that the cortical circuits of DSZ facilitate a modular integration of proprioceptive information along its major axis and disseminate this information to only selective parts of higher order somatic and MI cortices in parallel with cutaneous information. J. Comp. Neurol. 521:2585–2601, 2013. © 2013 Wiley Periodicals, Inc.