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Mnemonic representations of transient stimuli and temporal sequences in the rodent hippocampus in vitro

Abstract

A primary function of the brain is the storage and retrieval of information. Except for working memory, where extracellular recordings have shown persistent discharges during delay-response tasks, it has been difficult to link memories with changes in individual neurons or specific synaptic connections. We found that transient stimuli are reliably encoded in the ongoing activity of brain tissue in vitro. Patterns of synaptic input onto dentate hilar neurons predicted which of four pathways were stimulated with an accuracy of 76% and performed significantly better than chance for >15 s. Dentate gyrus neurons were also able to accurately encode temporal sequences using population representations that were robust to variation in sequence interval. These results demonstrate direct neural encoding of temporal sequences in the spontaneous activity of brain tissue and suggest a local circuit mechanism that may contribute to diverse forms of short-term memory.

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Figure 1: Persistent synaptic activity evoked by multiple perforant path stimuli.
Figure 2: Short-term hilar representations of multiple perforant path stimuli.
Figure 3: Prediction of stimulus identity from hilar population responses.
Figure 4: Time course of hilar population responses.
Figure 5: Visual display of cross-validated data.
Figure 6: Short-term representations of temporal sequences in hilar neurons.
Figure 7: Sequence representations are robust to perturbation of stimulus interval.
Figure 8: Population representations of stimulus and sequence identity in the dentate gyrus.

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Acknowledgements

We thank S. Solla for helpful discussions, and R. Galán and P. Larimer for comments on the manuscript. This work was supported by US National Institutes of Health grants NS33590 and DC04285. R.A.H. was supported by US National Institutes of Health training grant T32-GM007250.

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R.A.H. and B.W.S. designed the experiments, analyzed the data, prepared the figures and wrote the paper. R.A.H. performed all of the experiments.

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Correspondence to Ben W Strowbridge.

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Hyde, R., Strowbridge, B. Mnemonic representations of transient stimuli and temporal sequences in the rodent hippocampus in vitro. Nat Neurosci 15, 1430–1438 (2012). https://doi.org/10.1038/nn.3208

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