The rat vibrissal follicle-sinus complex is innervated by a deep vibrissal nerve (DVN) and several smaller fascicles traveling in the dermis [conus or superficial vibrissal nerves, (SVNs)]. The function of the SVNs is unknown, although it has been suggested in a comparative study that they form part of a diffuse, multivibrissal system. Anatomical and electrophysiological methods were used to test this hypothesis and to determine if DVN and SVN fibers have differing response profiles. No ganglion cells were double-labeled after retrograde tracer injections in the DVN and SVNs of single follicles. Electron microscopy showed that selective transection of the DVN caused no SVN degeneration or vice versa. Thus, the dual innervation of the vibrissa arises from separate ganglion cells that project through separate nerves. Ganglion cells with A-row vibrissa receptive fields were studied before and after cutting the DVN and/or SVNs to the responsive vibrissa in order to identify their peripheral trajectories. In this sample, 83% projected through a DVN and 17% via a SVN. SVN or DVN cells were not spontaneously active. All cells responded to single vibrissae only; none were responsive to intervibrissal hairs or skin. Latencies to electrical stimulation were similar for DVN and SVN cells. Adaptation rates and threshold measurements were also similar in the two groups: 60% of the DVN cells and 80% of the SVN cells gave slowly adapting responses to sustained vibrissal displacement; threshold displacements ranged from less than 1 degrees to greater than 15 degrees for both SVN and DVN cells. Direction sensitivity was found in all DVN and SVN slowly adapting cells, with most cells responding to movements in one or two quadrants. For SVN cells, sequential circumferential nerve sections indicated that the fiber's directional sensitivity matched the direction of the fiber's entry into the follicle. The two groups differed in their responses to pushing in or pulling on the hair shaft. All the DVN cells were responsive to both of these stimuli, while for SVN cells pushing activated only 40% and none were responsive to pulling the hair. Another difference in the two groups was that no injury discharges occurred after cutting SVNs, but were present in 44% of DVN cells. These data suggest that DVN and SVNs are similar in the majority of response properties. There is also no evidence to support the hypothesis that SVNs provide diffuse, multivibrissal inputs.