The organization of corticothalamic projections: reciprocity versus parity

All neocortical areas receive inputs from and project back to the thalamus. It is often said that the corticothalamic projections are organized in a way that reciprocates the spatial distribution of thalamocortical pathways. The present review examines to what extent this rule of reciprocity is actually supported by the most recent neuroanatomical data, particularly those relating to the central organization of the vibrissal sensory system in the rat. A critical survey of previous studies is made and new results are presented concerning the fine-grained organization of corticothalamic projections in this sensory system. Together, prior results and the present set of new data confirm the existence of both, reciprocal and nonreciprocal patterns of corticothalamic connectivity. This conclusion leads us to propose that the spatial organization of corticothalamic connections complies with a more fundamental rule, the rule of parity, from which reciprocity follows as a general, but not obligatory consequence. The rule of parity states that the distribution of corticothalamic projections across and within the thalamic nuclei is determined by the branching patterns of the different classes of prethalamic afferents. The anatomical, developmental and physiological consequences of this rule are discussed. The rule of parity suggests that, according to the behavioral context, both prethalamic and corticothalamic pathways may function in a feedback mode.