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Pattern Completion and Pattern Separation Mechanisms in the Hippocampus

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The Neurobiological Basis of Memory

Abstract

The mechanisms for pattern completion and pattern separation are described in the context of a theory of hippocampal function in which the hippocampal CA3 system operates as a single attractor or autoassociation network to enable rapid, one-trial associations between any spatial location (place in rodents, or spatial view in primates) and an object or reward, and to provide for completion of the whole memory during recall from any part. The factors important in the pattern completion in CA3 together with a large number of independent memories stored in CA3 include a sparse distributed representation which is enhanced by the graded firing rates of CA3 neurons, representations that are independent due to the randomizing effect of the mossy fibers, heterosynaptic long-term depression as well as long-term potentiation in the recurrent collateral synapses, and diluted connectivity to minimize the number of multiple synapses between any pair of CA3 neurons which otherwise distort the basins of attraction. Recall of information from CA3 is implemented by the entorhinal cortex perforant path synapses to CA3 cells, which in acting as a pattern associator allow some pattern generalization. Pattern separation is performed in the dentate granule cells using competitive learning to convert grid-like entorhinal cortex firing to place-like fields. Pattern separation in CA3, which is important for completion of any one of the stored patterns from a fragment, is provided for by the randomizing effect of the mossy fiber synapses to which neurogenesis may contribute, by the large number of dentate granule cells each with a sparse representation, and by the sparse independent representations in CA3. Recall to the neocortex is achieved by a reverse hierarchical series of pattern association networks implemented by the hippocampo-cortical backprojections, each one of which performs some pattern generalization to retrieve a complete pattern of cortical firing in higher-order cortical areas.

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Acknowledgments

Different parts of the research described here were supported by Program Grants from the Medical Research Council, by a Human Frontier Science Program Grant, by an EEC BRAIN grant, by the MRC Oxford Interdisciplinary Research Centre in Cognitive Neuroscience, by the Oxford McDonnell-Pew Centre in Cognitive Neuroscience, and by the Oxford Centre for Computational Neuroscience. The author has performed the experimental and theoretical work which is incorporated in some of the ideas presented here on the hippocampus with many colleagues, including Alessandro Treves, Simon Stringer, Ray Kesner, Robert Robertson, Pierre Georges-François, Shane O’Mara, and Alain Berthoz, and their contributions are sincerely acknowledged. Pdfs of some of the papers cited are available at www.oxcns.org.

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  1. Department of Computer Science and Oxford Centre for Computational Neuroscience, University of Warwick, CV4 7AL, Coventry, UK

    Prof. Edmund T. Rolls PhD, DSc

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  1. Prof. Edmund T. Rolls PhD, DSc
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Correspondence to Edmund T. Rolls PhD, DSc .

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Editors and Affiliations

  1. Department of Psychology, Radford University, Radford, Virginia, USA

    Pamela A. Jackson

  2. Department of Cognitive Science, University of California-San Diego, La Jolla, California, USA

    Andrea A. Chiba

  3. Department of Neurological Surgery and Center for Neuroscience, University of California-Davis, Davis, California, USA

    Robert F. Berman

  4. Department of Psychology, University of Illinois at Chicago, Chicago, Illinois, USA

    Michael E. Ragozzino

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Rolls, E. (2016). Pattern Completion and Pattern Separation Mechanisms in the Hippocampus. In: Jackson, P., Chiba, A., Berman, R., Ragozzino, M. (eds) The Neurobiological Basis of Memory. Springer, Cham. https://doi.org/10.1007/978-3-319-15759-7_4

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