Nonrandom Local Circuits in the Dentate Gyrus

By P. Larimer, B. Strowbridge. 2008

120 citations recorded by the source corpus.

The dentate hilus has been extensively studied in relation to its potential role in memory and in temporal lobe epilepsy. Little is known, however, about the synapses formed between the two major cell types in this region, glutamatergic mossy cells and hilar interneurons, or the organization of local circuits involving these cells. Using triple and quadruple simultaneous intracellular recordings in rat hippocampal slices, we find that mossy cells evoke EPSPs with high failure rates onto hilar neurons. Mossy cells show profound synapse specificity; 87.5% of their intralamellar connections are onto hilar interneurons. Hilar interneurons also show synapse specificity and preferentially inhibit mossy cells; 81% of inhibitory hilar synapses are onto mossy cells. Hilar IPSPs have low failure rates, are blocked by the GABAA receptor antagonist gabazine, and exhibit short-term depression when tested at 17 Hz. Surprisingly, more than half (57%) of the mossy cell synapses we found onto interneurons were part of reciprocal excitatory/inhibitory local circuit motifs. Neither the high degree of target cell specificity, nor the significant enrichment of structured polysynaptic local circuit motifs, could be explained by nonrandom sampling or somatic proximity. Intralamellar hilar synapses appear to function primarily by integrating synchronous inputs and presynaptic burst discharges, allowing hilar cells to respond over a large dynamic range of input strengths. The reciprocal mossy cell/interneuron local circuit motifs we find enriched in the hilus may generate sparse neural representations involved in hippocampal memory operations.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

Hilar Mossy Cell Degeneration Causes Transient Dentate Granule Cell Hyperexcitability and Impaired Pattern Separation (2012, unknown): “Excitation of mossy cells in vitro slices excites granule cells weakly but inhibits granule cells disynaptically via excitation of inhibitory interneurons (Scharfman, 1995; Larimer and Strowbridge, 2008), a finding consistent with the earlier in vivo results.”
Functional analysis of a higher olfactory center, the lateral horn (2012, background): “This idea has also influenced thinking about the role of inhibition in the mammalian cortex (Larimer and Strowbridge, 2008; Poo and Isaacson, 2009; Stokes and Isaacson, 2010).”
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition (2010, background): “Connectivity in a local cortical network is not completely random (149, 554, 699, 892).”
Dendrites of dentate gyrus granule cells contribute to pattern separation by controlling sparsity (2016, methodology): “As experimental data were obtained in the presence of synaptic activity blockers, a somatic current injection at the model cell was used to replicate those conditions.”