This study investigated the relationship between axonal projections and receptive field properties of whisker-sensitive cells in the principal trigeminal sensory nucleus of the rat. The labeling of small groups of trigeminothalamic axons with biotinylated dextran amine disclosed two broad classes of axons; a majority of fibers (68%; n = 107) project to a single barreloid of the ventral posteromedial nucleus, and the remaining group includes axons that innervate both the posterior group of the thalamus and the tectum. Additional terminal sites for axons of this latter group may include the pretectum, the zona incerta, the medial part of the medial geniculate nucleus, and the ventral posteromedial nucleus. Corresponding to these two classes of fibers, 67% of the cells in the principal trigeminal nucleus (n = 313) have single-whisker receptive fields, whereas the rest of the population have receptive fields composed of multiple whiskers. The tonic or phasic properties of the responses apparently bear no relation to the axonal projection patterns. Solid retrograde labeling of cells that project to the ventral posteromedial nucleus and intracellular staining revealed that single-whisker cells have small somata and narrow, barrelette-bounded dendritic trees. In contrast, multi-whisker neurons have large multipolar somata, expansive dendritic trees, and many respond antidromically to stimulation of the superior colliculus. Together, these results provide evidence for two main channels of vibrissal information: a single-whisker channel that links trigeminal barrelettes to their corresponding barreloids, and a multi-whisker channel that distributes principally in the posterior group and tectum.