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Multistability of cognitive maps in the hippocampus of old rats

Abstract

Hippocampal neurons provide a population code for location1. In young rats, environments are reliably ‘mapped’ by groups of neurons that have firing locations (‘place fields’2) that can be stable for several months3. Old animals exhibit deficits in spatial memory, raising the question of whether the quality or stability of their hippocampal ‘cognitive maps’4 is altered. By recording from large groups of neurons, we observed the hippocampal spatial code to be multistable. In young rats, the place field maps were reliable both within and between episodes in a familiar environment. In old rats, place field maps were accurate and stable during an episode, but frequently exhibited complete rearrangements between episodes. In a spatial memory task, both young and old rats exhibited bimodal performance, consistent with map multistability early in training. However, the performance of young rats became almost unimodal with further training, whereas that of old rats remained markedly bimodal. The multistability of the hippocampal map provides an insight into the dynamics of neural coding in high-level cortical structures and their changes during ageing, and may provide an explanation for the frequent failure of place recognition in elderly humans.

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Figure 1: Place-field distributions from one young and one old rat recorded on two consecutive episodes of running on a rectangular figure-8 maze.
Figure 2: Frequency distributions of average place-field correlations between maze episodes in the (r(between episodes)) for all recording sessions in all rats.
Figure 3: Mean performance scores (CIPL; see Methods) versus trial number for 98 young and 93 old rats on the Morris water task.

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Acknowledgements

We thank R. D'Monte, J. L. Gerrard, W. E. Skaggs, K. Stengel, J. Wang and K.L.Weaver for assistance with data acquisition and analysis; P. J. Best, D. Chialvo, L. Nadel, W. E. Skaggs and F. A. Wilson for comments on the manuscript, and D. Clayman for instigating the NIA extramural program through which this work was supported. This work was supported by NIA and NIMH.

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Correspondence to Carol A. Barnes.

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Barnes, C., Suster, M., Shen, J. et al. Multistability of cognitive maps in the hippocampus of old rats. Nature 388, 272–275 (1997). https://doi.org/10.1038/40859

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