We have physiologically characterized the receptive field properties of lamina I projection neurons with cutaneous input in the lumbar spinal cords of control rats and rats with unilateral adjuvant-induced inflammation of the hindlimb. The majority of cells recorded in rats with inflamed limbs demonstrated properties uncharacteristic of this cell population in control rats, including large receptive fields, discontinuous receptive fields, responsiveness to deep as well as cutaneous tissues and ongoing or bursting spontaneous activity. Cells with complex receptive fields were encountered from less than 6 h to 5 days after induction of inflammation. This time course correlates with the occurrence of hyperalgesia to thermal stimuli. The contributions of nociceptive afferent sensitization and alterations in the physical environment of peripheral receptors to the observed enlargement of receptive fields were examined by testing the responses of cells to localized electrical and thermal stimuli in the absence and presence of local anesthesia. Nociceptive primary afferents did not demonstrate enlarged receptive fields in this model of inflammation. The results imply that the enlargement of receptive fields cannot be accounted for by peripheral sensitization of peripheral nociceptors or physical changes in the environment of peripheral receptors and must therefore involve changes within the central nervous system.