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Long-term plasticity in hippocampal place-cell representation of environmental geometry

Nature volume 416, pages 90–94 (2002)Cite this article

Abstract

The hippocampus is widely believed to be involved in the storage or consolidation of long-term memories1,2,3,4. Several reports have shown short-term changes in single hippocampal unit activity during memory and plasticity experiments5,6,7,8,9,10,11,12, but there has been no experimental demonstration of long-term persistent changes in neuronal activity in any region except primary cortical areas13,14,15,16. Here we report that, in rats repeatedly exposed to two differently shaped environments, the hippocampal-place-cell representations of those environments gradually and incrementally diverge; this divergence is specific to environmental shape, occurs independently of explicit reward, persists for periods of at least one month, and transfers to new enclosures of the same shape. These results indicate that place cells may be a neural substrate for long-term incidental learning, and demonstrate the long-term stability of an experience-dependent firing pattern in the hippocampal formation.

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Figure 1: Similarity of spatial firing during early exposure to circular- and square-walled enclosures.
Figure 2: Repeated exposure to circle and square enclosures increases place field divergence.
Figure 3: Schematic (a) and observed (b, c, d) incremental development of divergent firing in individual place cells. ‘Ci → Sq’ denotes transformed-circle firing-rate maps (see Methods).
Figure 4: Shape-specific firing patterns learned in one type of enclosure were reproduced in different enclosures of similar shape.

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Acknowledgements

We thank J. Huxter, T. Hartley and K. Jeffery for discussion, S. Burton for reviewing the manuscript, C. Parker for technical assistance, and J. Donnett for the recording system. This work was supported by a Medical Research Council (UK) programme grant to J.O.K., MRC Advanced Studentships to C.L. and T.W., a Wellcome Trust Studentship to F.C., and Royal Society and MRC Senior Fellowships to N.B.

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Authors and Affiliations

  1. Department of Anatomy and Developmental Biology, University College London, WC1E 6BT, UK

    Colin Lever, Tom Wills, Francesca Cacucci, Neil Burgess & John O'Keefe

  2. Institute of Cognitive Neuroscience, University College London, WC1E 6BT, UK

    Neil Burgess & John O'Keefe

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  1. Colin Lever
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  2. Tom Wills
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Correspondence to Colin Lever or John O'Keefe.

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Lever, C., Wills, T., Cacucci, F. et al. Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416, 90–94 (2002). https://doi.org/10.1038/416090a

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