Recent studies with kindling and convulsant drug models of epilepsy suggest that the piriform (primary olfactory) cortex may be particularly susceptible to generation of epileptiform activity. The present study has examined the generation of interictal epileptiform events in the piriform cortex of kindled rats in vivo, taking advantage of special features of this system that facilitate physiological analysis. The investigation included analysis of extracellular and intracellular potentials, and membrane currents computed by current source density (CSD) analysis. In pyramidal cells, epileptiform events consisted of an initial EPSP that occurred in all-or-none fashion and a long-lasting IPSP with Cl(-)- and K(+)-mediated components. Onset of the IPSP was sufficiently fast that firing evoked by the EPSP was consistently limited to single action potentials. CSD analysis revealed the presence of two distinctly different excitatory epileptiform currents: an initial inward current of unknown origin that is widely distributed over depth, and a second much larger inward current at the depths of proximal apical and basal dendrites of pyramidal cells. It was concluded that this second component is mediated by the associational projections of pyramidal cells excited by the first component. Since these heavy associational projections also extend to neighboring areas including the amygdala, entorhinal cortex, and insular and orbitofrontal areas of neocortex, this second component could be widely propagated within the basal forebrain. An important finding was that the EPSP generated by this associational pathway was completely blocked in cell bodies of pyramidal cells in piriform cortex by the IPSP during most events. This IPSP may therefore play a critical role in limiting seizure activity by preventing reverberating positive feedback in the pyramidal cell population. It can be speculated that compromise of this IPSP, as by repetitive activation by the shock trains used for kindling, leads to prolonged epileptic activity in the piriform cortex and the many limbic structures to which it projects.