Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3

Abstract

The hippocampus, a critical brain structure for navigation, context-dependent learning and episodic memory1,2,3, is composed of anatomically heterogeneous subregions. These regions differ in their anatomical inputs as well as in their internal circuitry4. A major feature of the CA3 region is its recurrent collateral circuitry, by which the CA3 pyramidal cells make excitatory synaptic contacts on each other4,5. In contrast, pyramidal cells in the CA1 region are not extensively interconnected4. Although these differences have inspired numerous theoretical models of differential processing capacities of these two regions6,7,8,9,10,11,12,13, there have been few reports of robust differences in the firing properties of CA1 and CA3 neurons in behaving animals. The most extensively studied of these properties is the spatially selective firing of hippocampal ‘place cells’1,14. Here we report that in a dynamically changing environment, in which familiar landmarks on the behavioural track and along the wall are rotated relative to each other15,16, the population representation of the environment is more coherent between the original and cue-altered environments in CA3 than in CA1. These results demonstrate a functional heterogeneity between the place cells of CA3 and CA1 at the level of neural population representations.

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Figure 1: Experimental design.
Figure 2: Individual place field responses to cue manipulations.
Figure 3: Correlation matrices between population firing rate vectors.
Figure 4: Ensemble coherence.

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Acknowledgements

This study was supported by the National Institute of Neurological Disorders and Stroke, the National Institute of Mental Health, and the Lucille P. Markey Charitable Trust. We thank E. Moser and A. Treves for comments and discussion. We also thank E. Hargreaves for assistance in collecting data for Supplementary Figs 5 and 6. G.R. and D.Y. assisted in data collection and behavioural training throughout the experiments.

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Correspondence to Inah Lee or James J. Knierim.

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Supplementary information

Supplementary Figure 1

This figure shows the proportion of place field response types for each animal in the sample. (DOC 136 kb)

Supplementary Figure 2

This figure describes the technique for creating the correlation matrices between population vectors of firing rates in two recoding sessions. (DOC 216 kb)

Supplementary Figure 3

This figure shows the relationship between the amount of cue mismatch and (a) the maximum population vector correlations and (b) the length of the vector denoting the mean rotation angle of the population. (DOC 217 kb)

Supplementary Figure 4-6

These 3 figures show supplementary analyses and data to demonstrate that CA3 place fields could be affected by the distal landmarks, even though in the main experiment their firing fields were dominated by the local cues on the track. (DOC 1841 kb)

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Lee, I., Yoganarasimha, D., Rao, G. et al. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430, 456–459 (2004). https://doi.org/10.1038/nature02739

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