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Cited by 545Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

The mechanisms for pattern completion and pattern separation in the hippocampus

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Rolls, Edmund T.·2013·Frontiers in Systems Neuroscience
DOI 10.3389/fnsys.2013.00074PMC PMC3812781
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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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  • The failure in the use of a strategy based on local cues after massive modification of the global shape of the surrounding environment could be indicative of the triggering of a global remapping that leads subjects to perceive the substantially altered experimental setup as a novel environment.

    “The failure in the use of a strategy based on local cues after the massive modification of the global shape of the surrounding environment could be indicative of the triggering of a global remapping that lead the subjects to perceive the substantially altered experimental setup as a novel environment”

    From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [80]

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  • This feature seems to depend on a pattern completion mechanism that is able to reinstate complete memories after partial cueing, based on the operation of hippocampal autoassociative neural networks.

    “This feature seems to depend on a pattern completion mechanism that is able to reinstate complete memories after partial cueing, based on the operation of hippocampal autoassociative neural networks”

    From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [80]

  • In mammals, similar spatial behavior capabilities likely depend on dentate gyrus to CA3 projections operating as a sparse coding device that performs pattern separation during initial encoding and memory storage.

    “It has been proposed [79,80,190,206,207] that similar spatial behavior capabilities likely depend, in mammals, on two hypothetical hippocampal mechanisms: first, the projections from the dentate gyrus to the CA3 area of the hippocampus seem to operate as a sparse coding device that orthogonalizes and disambiguates similar inputs patterns, performing pattern separation during initial encoding and”

    From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [80]

  • In mammals, similar spatial behavior capabilities likely depend on the extensive recurrent-collateral network of CA3 neurons operating as an autoassociative network that stores arbitrary associations between stimuli and functions as a pattern completion mechanism.

    “second, the extensive recurrent-collateral network of the CA3 neurons operates as an autoassociative network that allows the storage of arbitrary associations between stimuli, and that functions as a pattern completion mechanism that reinstates the complete memories in response to incomplete input patterns.”

    From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [80]

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  1. Amaral D. G. Price J. L. Pitkanen A. Carmichael S. T. (1992). Anatomical organization of the primate amygdaloid complex, in The Amygdala, ed Aggleton J. P. (New York, NY: Wiley-Liss), 1– 66
  2. Morris R. G. M. (1989). Does synaptic plasticity play a role in information storage in the vertebrate brain? in Parallel Distributed Processing: Implications for Psychology and Neurobiology, ed Morris R. G. M. (Oxford: Oxford University Press), 248– 285
  3. Rolls E. T. (1987). Information representation, processing and storage in the brain: analysis at the single neuron level, in The Neural and Molecular Bases of Learning, eds Changeux J.-P. Konishi M. (Chichester: Wiley), 503– 540
  4. Rolls E. T. (1989a). Functions of neuronal networks in the hippocampus and cerebral cortex in memory, in Models of Brain Function, ed Cotterill R. M. J. (Cambridge: Cambridge University Press), 15– 33
  5. Schultz S. Panzeri S. Rolls E. T. Treves A. (2000). Chap. 14. Quantitive model analysis of a Schaffer collateral model, in Information Theory and the Brain, ed Hancock P. Foldiak P. Baddeley R. (Cambridge: Cambridge University Press), 257– 272
  6. Storm-Mathiesen J. Zimmer J. Ottersen O. P. (eds.). (1990). Understanding the Brain Through the Hippocampus. Oxford: Elsevier
  7. Witter M. P. Naber P. A. Van Haeften T. Machielsen W. C. Rombouts S. A. Barkhof F. (2000a). Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10, 398– 410 10.1002/1098-1063(2000)10:4<398::AID-HIPO6>3.3.CO;2-B 10985279 · DOI

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Authors
Rolls, E. T.
Affiliations
University of Warwick (GB)
Corresponding author
Rolls, Edmund T.
ORCID
Rolls, Edmund T.
Venue
Frontiers in Systems Neuroscience
Publisher
Frontiers Media SA
Published
2013
Volume
7
Pages
74-74
ISSN
1662-5137 (ISSN-L)
DOI
10.3389/fnsys.2013.00074
PMC
PMC3812781
OpenAlex
W2016454630
Cited by
545
References
191
Citations by year
2026: 55 · 2025: 66 · 2024: 49 · 2023: 42 · 2022: 42 · 2021: 77 · 2020: 42 · 2019: 30 · 2018: 34 · 2017: 32 · 2016: 33 · 2015: 29 · 2014: 12 · 2013: 2
FWCI
2.15
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Systems Neuroscience (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Medical Research Council
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
pattern completion, pattern separation, hippocampus, CA3, attractor networks, autoassociation, sparse distributed representations, mossy fibers, long-term potentiation, dentate gyrus granule cells, entorhinal cortex, perforant path, place cells, grid cells, pattern generalization, neurogenesis, memory retrieval

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