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Segmentation of spatial experience by hippocampal theta sequences

Abstract

The encoding and storage of experience by the hippocampus is essential for the formation of episodic memories and the transformation of individual experiences into semantic structures such as maps and schemas. The rodent hippocampus compresses ongoing experience into repeating theta sequences, but the factors determining the content of theta sequences are not understood. Here we first show that the spatial paths represented by theta sequences in rats extend farther in front of the rat during acceleration and higher running speeds and begin farther behind the rat during deceleration. Second, the length of the path is directly related to the length of the theta cycle and the number of gamma cycles in it. Finally, theta sequences represent the environment in segments or 'chunks'. These results imply that information encoded in theta sequences is subject to powerful modulation by behavior and task variables. Furthermore, these findings suggest a potential mechanism for the cognitive 'chunking' of experience.

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Figure 1: Distinct populations of theta sequences on the two-choice T maze.
Figure 2: Examples of ahead sequences while rats were located at the choice point.
Figure 3: Examples of ahead and behind sequences.
Figure 4: Characteristics of theta sequence ahead and behind length.
Figure 5: Theta period and gamma cycles vary as functions of path length.
Figure 6: Ahead length, behind length and path distribution vary according to landmarks on the maze.
Figure 7: Segmented representation of space by theta sequences.
Figure 8: Relationships between rat behavior and the represented path.

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Acknowledgements

We thank C. Boldt, K.D. Seeland and A.P. Steiner for technical assistance and A. Johnson and the members of the Redish lab for discussion. This work was supported by US National Institutes of Health grants (R01 MH-080318 and F30 MH-091821), the Pennsylvania Department of Health and a US National Science Foundation Integrative Graduate Education and Research Traineeship grant (DGE-0549352).

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A.S.G., M.A.A.v.d.M. and A.D.R. designed the experiment; D.S.T. and A.D.R. supervised the project; A.S.G. and M.A.A.v.d.M. carried out the experiments; A.S.G. analyzed the data; and A.S.G., M.A.A.v.d.M., D.S.T. and A.D.R. wrote the paper.

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Correspondence to A David Redish.

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Gupta, A., van der Meer, M., Touretzky, D. et al. Segmentation of spatial experience by hippocampal theta sequences. Nat Neurosci 15, 1032–1039 (2012). https://doi.org/10.1038/nn.3138

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