Neurons located in the zona incerta (ZI) of the ventral thalamus project to several regions of the central nervous system, including the neocortex, superior colliculus, and brainstem. However, whether these projections are functionally segregated remains unknown. This issue was addressed here by combining neuroanatomical tracers with immunohistochemical staining for gamma-aminobutyric acid (GABA) and/or parvalbumin, coupled with neurophysiological mapping. GABAergic projection neurons were found in four distinct subregions of the ZI including: (1) the rostral pole of the ZI, from which neurons project to the supragranular layers of the neocortex (especially layer I); (2) the dorsal subregion of the ZI, where both ascending projections to the neocortex and descending projections to the pretectal area were observed; (3) the ventral subregion of the ZI, whose neurons project to the superior colliculus; and 3) the caudal pole of the ZI, from which descending projections to the lower brainstem and spinal cord were observed. Somatotopic representations of the contralateral cutaneous periphery were also identified in the dorsal and ventral subregions of ZI, both of which were found to receive dense direct afferent projections from the trigeminal complex, and dorsal column nuclei. These results suggest that the rat ZI is a major somatosensory relay in the ventral thalamus, carrying feed-forward inhibitory signals to neocortical and subcortical targets, in parallel with the excitatory somatosensory pathways.