We have used single unit recording techniques to map the representation of cutaneous and joint somatosensory modalities in the primary somatosensory (SI) cortex of both anesthetized and awake rats. The cytoarchitectonic zones within the rat SI were divided into the following main categories: (1) granular zones (GZs)--areas exhibiting koniocortical cytoarchitecture (i.e., containing dense aggregates of layer IV granule cells), (2) perigranular zones (PGZs)--narrow strips of less granular cortex surrounding the GZs, and (3) dysgranular zones (DZs)--large areas of dysgranular cortex enclosed within the SI. The narrow strip between the SI and the rostrally adjacent frontal agranular cortex was termed the "transitional zone" (TZ). Initial computer-based studies of the properties of cutaneous receptive fields (RFs) in SI showed that, although there were differences in response threshold, adaptability, frequency response, and overall RF size and shape of adjacent neurons, the size and location of the "centers" of the RFs were quite constant and were similar to those seen in multiple unit recordings. The same was true of RFs of single neurons recorded through different anesthetic states. The body representation in SI was first mapped by determining single unit and unit cluster RFs within a total of 2,170 microelectrode penetrations in barbiturate-anesthetized rats. Cutaneous RFs in the GZs were quite discrete. Thus, a single, finely detailed, continuous map of the cutaneous periphery was definable within the GZs themselves. Only the forepaw had a double representation. RFs in the PGZs were larger and more diffuse, but since they covered roughly the same skin areas as the RFs in the most closely adjacent GZs, they fit into the same body map. Neurons in the DZs were unresponsive to any sensory stimuli in the anesthetized animal. In chronically implanted, freely moving, awake animals cutaneous RFs were larger and more volatile than in the anesthetized, but the accuracy of the map was clearly preserved by the fact that the locations of the RF centers (which often must be defined quantitatively) were unchanged. The PGZs and DZs in the awake animals exhibited a multimodal convergence of cutaneous and joint movement RFs within single vertical penetrations, or even on single neurons. Directionally specific and bilateral cutaneous RFs were also observed in the DZs. It was concluded the DZs are more associational or integrative areas within the SI, but they could not be shown to comprise a distinct and separate body representation.(ABSTRACT TRUNCATED AT 400 WORDS)