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Independent rate and temporal coding in hippocampal pyramidal cells

Abstract

In the brain, hippocampal pyramidal cells use temporal1 as well as rate2 coding to signal spatial aspects of the animal's environment or behaviour. The temporal code takes the form of a phase relationship to the concurrent cycle of the hippocampal electroencephalogram theta rhythm1. These two codes could each represent a different variable3,4. However, this requires the rate and phase to vary independently, in contrast to recent suggestions5,6 that they are tightly coupled, both reflecting the amplitude of the cell's input. Here we show that the time of firing and firing rate are dissociable, and can represent two independent variables: respectively the animal's location within the place field, and its speed of movement through the field. Independent encoding of location together with actions and stimuli occurring there may help to explain the dual roles of the hippocampus in spatial and episodic memory7,8, or may indicate a more general role of the hippocampus in relational/declarative memory9,10.

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Figure 1: Place cell phase of firing correlates best with position.
Figure 2: Phase precession is independent of IFR.
Figure 3: Phase is correlated with track location on low- as well as high-firing-rate runs.
Figure 4: Firing rates differ on fast and slow runs through the field.
Figure 5: Phase precession on the shortened tracks.

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Acknowledgements

We thank C. Lever, F. Cacucci, T. Wills, J. Ryan, D. Edwards and T. Hartley for technical assistance. This work was supported by the MRC and the Wellcome Trust. J.H. was a Rothermere Fellow.

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Correspondence to John O'Keefe.

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Huxter, J., Burgess, N. & O'Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828–832 (2003). https://doi.org/10.1038/nature02058

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