The carotid body is a major sensor of oxygen partial pressure in the arterial blood, and plays a role in the control of respiration. Despite extensive investigation of the structure, the cellular basis of the transduction mechanism remains poorly understood. We have developed a preparation of freshly dissociated cells from the rabbit carotid body, in which two cell types may be identified using morphological criteria. The preparation allows application of the patch clamp technique to characterize the properties of the cells which have otherwise proved difficult to study in situ. Carotid bodies of rabbits were dissociated using a combination of enzymatic and mechanical procedures. The dissociated preparation obtained consisted of clusters of spherical or ovoid cells of 12-15 microns in diameter and a distinct population of spherical cells of 8-10 microns diameter. Electron microscopic techniques were used to identify the cells present in the preparation. Again two populations of cells could be distinguished. A population of cells 10-12 microns in diameter, often found in clusters, possessed the dense-cored vesicles characteristic of Type I cells, while a population of smaller cells (diameter 5-7 microns) had peripherally condensed nuclear chromatin and fine cytoplasmic surface extensions characteristic of Type II cells. Patch clamp study of the cells showed that they represent two electrophysiologically distinct populations. The larger cells, corresponding to Type I cells, were found to be excitable, generating fast, sodium-dependent action potentials that were recorded both in the cell attached and whole cell recording configurations. The smaller Type II cells did not generate action potentials. Voltage clamp study of Type I cells allowed definition of a range of voltage-gated currents. These included an inactivating, tetrodotoxin-sensitive inward sodium current, a high threshold sustained inward calcium current, and outward potassium currents. A component of the outward current showed a dependence on voltage-gated calcium entry, and was blocked by cobalt or cadmium. Of the calcium-dependent current, a component was sensitive to apamin, and the remaining current was blocked by tetraethylammonium. Type II cells showed only a high threshold outward potassium current. These studies have thus revealed an electrophysiological differentiation that parallels the morphological differentiation of the cells of the carotid body. The Type I cell is essentially neuron-like in its properties, while the Type II cell appears to have properties resembling those of glial elements elsewhere in the nervous system.(ABSTRACT TRUNCATED AT 400 WORDS)