A recent study has described synchronous burst discharges of dentate hilar neurons and area CA3 pyramidal cells in the presence of the convulsants 4-aminopyridine and picrotoxin in guinea-pig hippocampal slices [Müller W. and Misgeld U. (1991) J. Neurophysiol. 65, 141-147]. To examine the synchronous activity of dentate cells and area CA3 pyramidal cells further, epileptiform burst discharges were examined in morphologically and/or electrophysiologically identified non-granule cells in the hilus and granule cell layer of the rat dentate gyrus and compared to simultaneously-recorded pyramidal cells of area CA3a, b, and c. Specifically, the types of dentate cells and the types of discharge were examined, as well as the timing of burst discharge of dentate cells relative to different cells of area CA3. In the presence of the GABAA receptor antagonist bicuculline (30 microM), all dentate cell types discharged in rhythmic, spontaneous bursts that were synchronized with area CA3 pyramidal cell epileptiform bursts. The sampled cells included hilar "mossy" cells, hilar fast-spiking cells (putative interneurons) as well as interneurons located in the granule cell layer, such as the pyramidal "basket" cells. Simultaneous recording from dentate non-granule cells and area CA3 pyramidal cells during exposure to bicuculline demonstrated that stimulus-evoked and spontaneous epileptiform bursts occurred almost exactly at the same time; there were only a few milliseconds between the onsets of pyramidal cell bursts and dentate cell bursts, with the pyramidal cell preceding the dentate cell in almost every case. There were no systematic differences among dentate cell types in the extent they lagged behind pyramidal cells, and there were no detectable differences among area CA3 pyramidal cells. In slices that were cut between area CA3 and the dentate gyrus, epileptiform bursts occurred in area CA3 but not in the dentate. These findings suggest that, in the absence of GABAA receptor-mediated inhibition, excitatory pathways from area CA3 to the dentate gyrus are strong and widespread. These pathways, and possibly other mechanisms, can lead to tightly synchronized action potential discharge of pyramidal cells and dentate non-granule cells. The results also suggest that disinhibition alone is insufficient to cause synchronous bursts in the dentate gyrus, in contrast to area CA3.