Representing information in neuronal cell assemblies: Persistent activity in the dentate gyrus mediated by semilunar granule cells

Using rat hippocampal slices, we found that perforant path stimulation evokes long-lasting barrages of synaptic inputs in subpopulations of dentate gyrus mossy cells and hilar interneurons. Synaptic barrages could trigger persistent firing in hilar neurons. We found that synaptic barrages originate from semilunar granule cells (SGCs), glutamatergic neurons in the inner molecular layer that generate long-duration plateau potentials in response to excitatory synaptic input. MK801, nimodipine, and nickel all abolished stimulus-evoked plateau potentials in SGCs, and synaptic barrages in downstream hilar neurons, without blocking fast synaptic transmission. Hilar up-states triggered functional inhibition in granule cells that persisted for >10 s. Hilar cell assemblies, assayed by simultaneous triple and paired intracellular recordings, were linked by persistent firing in SGCs. Population responses recorded in hilar neurons accurately encoded stimulus identity. Stimulus-evoked up-states in dentate gyrus represent a potential cellular basis for hippocampal working memory.