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Remapping revisited: how the hippocampus represents different spaces

Abstract

The representation of distinct spaces by hippocampal place cells has been linked to changes in their place fields (the locations in the environment where the place cells discharge strongly), a phenomenon that has been termed ‘remapping’. Remapping has been assumed to be accompanied by the reorganization of subsecond cofiring relationships among the place cells, potentially maximizing hippocampal information coding capacity. However, several observations challenge this standard view. For example, place cells exhibit mixed selectivity, encode non-positional variables, can have multiple place fields and exhibit unreliable discharge in fixed environments. Furthermore, recent evidence suggests that, when measured at subsecond timescales, the moment-to-moment cofiring of a pair of cells in one environment is remarkably similar in another environment, despite remapping. Here, I propose that remapping is a misnomer for the changes in place fields across environments and suggest instead that internally organized manifold representations of hippocampal activity are actively registered to different environments to enable navigation, promote memory and organize knowledge.

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Fig. 1: Basic characteristics of place cell firing.
Fig. 2: Competitive networks and cofiring.
Fig. 3: Features and challenges to the standard view of place cell function.
Fig. 4: Registering internally organized population dynamics to allocentric influences.
Fig. 5: The reregistration concept.

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Acknowledgements

I thank J. Ranck Jr, a one-of-a-kind mentor who introduced the concepts of manifolds and differential topology to me during my graduate training, back when we only dreamed of recording ensembles. Thanks to the current and past members of my laboratory, especially S. Carrillo-Segura, D. Dvorak and E. Park with whom I discussed and argued about ideas in this Perspective. I am very grateful to J. Kubie for our many ‘cookie-cutter model’ discussions over the years, during which some of these Perspective ideas were born, and to G. Buzsáki and D. Heeger for critical comments on earlier drafts of the manuscript, and especially their encouragement to be brave.

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Fenton, A.A. Remapping revisited: how the hippocampus represents different spaces. Nat. Rev. Neurosci. (2024). https://doi.org/10.1038/s41583-024-00817-x

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