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Preplay of future place cell sequences by hippocampal cellular assemblies

Abstract

During spatial exploration, hippocampal neurons show a sequential firing pattern in which individual neurons fire specifically at particular locations along the animal’s trajectory (place cells1,2). According to the dominant model of hippocampal cell assembly activity, place cell firing order is established for the first time during exploration, to encode the spatial experience, and is subsequently replayed during rest3,4,5,6 or slow-wave sleep7,8,9,10 for consolidation of the encoded experience11,12. Here we report that temporal sequences of firing of place cells expressed during a novel spatial experience occurred on a significant number of occasions during the resting or sleeping period preceding the experience. This phenomenon, which is called preplay, occurred in disjunction with sequences of replay of a familiar experience. These results suggest that internal neuronal dynamics during resting or sleep organize hippocampal cellular assemblies13,14,15 into temporal sequences that contribute to the encoding of a related novel experience occurring in the future.

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Figure 1: Preplay of novel place cell sequences.
Figure 2: Quantification of the preplay phenomenon and comparison with replay.
Figure 3: Bayesian reconstruction of the animal’s trajectory in the familiar track (replay) and novel arm (preplay).
Figure 4: Preplay of novel place cell sequences before any linear track experience.

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Acknowledgements

We thank M. A. Wilson for assistance with data acquisition, discussions and comments on an earlier version of the manuscript; J. O’Keefe, A. Siapas, F. Kloosterman, D. L. Buhl for comments on earlier versions of the manuscript; and F. Kloosterman for providing assistance with the line detection for the Bayesian decoding. This work was supported by NIH grants R01-MH078821 and P50-MH58880 to S.T., who was an HHMI Investigator in an earlier part of this study.

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S.T. and G.D. conceived the project jointly. G.D. designed and performed the experiments and the analyses. G.D. and S.T. wrote the paper.

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Correspondence to George Dragoi or Susumu Tonegawa.

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The authors declare no competing financial interests.

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Dragoi, G., Tonegawa, S. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature 469, 397–401 (2011). https://doi.org/10.1038/nature09633

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