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Representing information in cell assemblies: persistent activity mediated by semilunar granule cells

Nature Neuroscience volume 13, pages 213–222 (2010)Cite this article

Abstract

Here we found that perforant path stimulation in rat hippocampal slices evoked long-lasting barrages of synaptic inputs in subpopulations of dentate gyrus mossy cells and hilar interneurons. Synaptic barrages triggered persistent firing in hilar neurons (hilar up-states). 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 both 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 more than 10 s. Hilar cell assemblies, identified 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 the dentate gyrus represent a potential cellular basis for hippocampal working memory.

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Figure 1: Long-lasting synaptic barrages in hilar neurons evoked by perforant path stimulation.
Figure 2: Hilar up-states require glutamatergic synaptic inputs.
Figure 3: Perforant pathway stimulation evokes plateau potentials and persistent firing in SGCs.
Figure 4: Correlation between plateau potentials in SGCs and hilar up-states following perforant pathway stimulation.
Figure 5: SGCs receive large glutamatergic inputs.
Figure 6: Plateau potentials in SGCs activated by NMDA receptors.
Figure 7: Both plateau potentials in SGCs and synaptic barrages in hilar neurons require L- and T-type VGCCs.
Figure 8: Perforant pathway-evoked up-states generate hilar cell assemblies that encode stimulus identity.

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Acknowledgements

We thank T. Pressler and R. Galán for helpful discussions; S. Jones and J. Frazier for helpful comments on the manuscript; and P. Puzerey for technical assistance. This work was supported by National Institutes of Health (NIH) Grant R01-NS33590 to B.W.S.

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  1. Department of Neurosciences, Case Western Reserve University, Cleveland, Ohio, USA

    Phillip Larimer & Ben W Strowbridge

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The study was designed, data analyzed and manuscript written by P.L. and B.W.S. The experimental work was performed by P.L.

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Correspondence to Ben W Strowbridge.

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Larimer, P., Strowbridge, B. Representing information in cell assemblies: persistent activity mediated by semilunar granule cells. Nat Neurosci 13, 213–222 (2010). https://doi.org/10.1038/nn.2458

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