A simple ordering of neocortical areas established by the compartmental organization of their striatal projections

The compartmental organization of corticostriatal projections from the fronto-orbito-insular cortex was studied in the cat. Cortical areas in this field were found to have a highly organized projection to the striatum, selectively innervating striosomes dorsally and predominantly avoiding them ventrally within their striatal fields of termination. These observations have two important implications for striatal processing. First, some cortical areas preferentially terminate in different compartments in different parts of the striatum. Therefore, the sources of input to striosomes and matrix are not categorical but switch according to the striatal region considered. Second, three properties of the bicompartmental termination pattern--one-dimensionality, common polarization, and multiple positions at which the pattern switched from "fills" to "avoids"--allowed us to order the corticostriatal projections with respect to one another. This ordering of the striatal projections of cortical areas implies an ordering of the cortical areas themselves, one that is independent of transcortical connections. For the corticostriatal projections described in this report, the ordering is [parietal, dorsomedial prefrontal, ventrolateral prefrontal, insular, rostral temporal] cortex. Our analysis suggests that a major function of striatal compartmentalization is to segregate and then bring together inputs from cortical areas at different positions in this ordering. The ordering may also serve as a simple format for specifying corticostriatal connections in development.