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Grid cells in pre- and parasubiculum

Abstract

Allocentric space is mapped by a widespread brain circuit of functionally specialized cell types located in interconnected subregions of the hippocampal-parahippocampal cortices. Little is known about the neural architectures required to express this variety of firing patterns. In rats, we found that one of the cell types, the grid cell, was abundant not only in medial entorhinal cortex (MEC), where it was first reported, but also in pre- and parasubiculum. The proportion of grid cells in pre- and parasubiculum was comparable to deep layers of MEC. The symmetry of the grid pattern and its relationship to the theta rhythm were weaker, especially in presubiculum. Pre- and parasubicular grid cells intermingled with head-direction cells and border cells, as in deep MEC layers. The characterization of a common pool of space-responsive cells in architecturally diverse subdivisions of parahippocampal cortex constrains the range of mechanisms that might give rise to their unique functional discharge phenotypes.

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Figure 1: Relative positions of pre- and parasubiculum in the rat brain.
Figure 2: Functional cell types of the presubiculum.
Figure 3: Functional cell types of the parasubiculum.
Figure 4: Functional cell types of MEC16.
Figure 5: Distribution of grid scores, mean vector length and border scores for the 630 MEC cells16, sorted by layers.
Figure 6: Grid spacing and grid orientation in local ensembles of grid cells in presubiculum and parasubiculum.
Figure 7: Theta modulation of functional cell types in presubiculum, parasubiculum and MEC.
Figure 8: Distribution of grid cells, theta-modulated cells and head direction–modulated cells in the parahippocampal cortex.

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Acknowledgements

We thank R. Skjerpeng for programming, D. Derdikman for help with code, J. Ainge for donating an implanted rat, and A.M. Amundgård, I. Hammer, K. Haugen, K. Jenssen and H. Waade for technical assistance. This work was supported by the Kavli Foundation and a Centre of Excellence grant from the Norwegian Research Council.

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C.N.B., F.S., M.P.W., E.I.M. and M.-B.M. planned and interpreted the study. M.-B.M. provided training and supervision. C.N.B., F.S. and T.S. performed surgeries. C.N.B. and M.P.W. performed histological reconstructions. C.N.B., F.S., V.H.T. and T.S. recorded the data. C.N.B., F.S., E.I.M. and M.-B.M. carried out the analyses. C.N.B. and E.I.M. wrote the paper. Data from a previous study16 were reanalyzed by C.N.B. and E.I.M.

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Correspondence to Edvard I Moser.

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Boccara, C., Sargolini, F., Thoresen, V. et al. Grid cells in pre- and parasubiculum. Nat Neurosci 13, 987–994 (2010). https://doi.org/10.1038/nn.2602

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