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The mechanisms for pattern completion and pattern separation in the hippocampus
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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 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”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [80]
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“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]
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“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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Self-citationA Specific Role of the Human Hippocampus in Recall of Temporal Sequences
Lehn, H., Steffenach, H.-A., van Strien, N. M., Veltman, D. J., Witter, M. P., & Haberg, A. K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5370-08.2009 · Cited by 187
Decision‐making and Weber's law: a neurophysiological model
Deco, G., & Rolls, E. T. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04940.x · Cited by 181
Self-citationInformation About Spatial View in an Ensemble of Primate Hippocampal Cells
Rolls, E. T., Treves, A., Robertson, R. G., Georges‐François, P., & Panzeri, S. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.4.1797 · Cited by 179
Self-citationInvariant Visual Object and Face Recognition: Neural and Computational Bases, and a Model, VisNet
Rolls, E. T. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00035 · Cited by 174
Self-citationNeural 'bubble' dynamics in two dimensions: foundations
Taylor, J. G. (1999) · Biological Cybernetics · doi:10.1007/s004220050534 · Cited by 172
Giocomo, L. M., & Hasselmo, M. E. (2007) · Molecular Neurobiology · doi:10.1007/s12035-007-0032-z · Cited by 165
Role of CA3 and CA1 subregions of the dorsal hippocampus on temporal processing of objects
Hoge, J., & Kesner, R. P. (2007) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.04.013 · Cited by 156
Sidhu, M. K., Stretton, J., Winston, G. P., Bonelli, S. B., Centeno, M., Vollmar, C., Symms, M. R., Thompson, P. J., Koepp, M. J., & Duncan, J. S. (2013) · Brain · doi:10.1093/brain/awt099 · Cited by 154
Spatial View Cells in the Primate Hippocampus: Effects of Removal of View Details
Robertson, R. G., Rolls, E. T., & Georges‐François, P. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.3.1145 · Cited by 153
Self-citationGilbert, P. E., & Kesner, R. P. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.6.1385 · Cited by 153
Graded-response neurons and information encodings in autoassociative memories
Treves, A. (1990) · Physical Review A · doi:10.1103/physreva.42.2418 · Cited by 149
An analysis of the dentate gyrus function
Kesner, R. P. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.01.012 · Cited by 148
Florian, C., & Roullet, P. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.03.003 · Cited by 146
Object, Space, and Object-Space Representations in the Primate Hippocampus
Rolls, E. T., Xiang, J.-Z., & Franco, L. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01063.2004 · Cited by 146
Self-citationPer, A., Morris, R., David, A., Tim, B., & O'Keefe, J. M. (2006) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195100273.003.0001 · Cited by 135
van Haeften, T., Baks‐te‐Bulte, L., Goede, P. H., Wouterlood, F. G., & Witter, M. P. (2003) · Hippocampus · doi:10.1002/hipo.10144 · Cited by 135
Reward-Spatial View Representations and Learning in the Primate Hippocampus
Rolls, E. T., & Xiang, J.-Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1481-05.2005 · Cited by 133
Self-citationHunsaker, M. R., & Kesner, R. P. (2008) · Hippocampus · doi:10.1002/hipo.20455 · Cited by 133
Rolls, E. T. (1989) · Addison-Wesley Longman Publishing Co., Inc. eBooks · Cited by 132
Self-citationA quantitative theory of the functions of the hippocampal CA3 network in memory
Rolls, E. T. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00098 · Cited by 124
Self-citationLavenex, P., SUZUKI, W. A., & Amaral, D. G. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20079 · Cited by 122
Delatour, B., & Witter, M. P. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01973.x · Cited by 117
Models of Grid Cell Spatial Firing Published 2005–2011
Zilli, E. A. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00016 · Cited by 109
Pitkänen, A., Kelly, J. L., & Amaral, D. G. (2002) · Hippocampus · doi:10.1002/hipo.1099 · Cited by 109
Emotion and decision-making explained: A précis
Rolls, E. T. (2014) · Cortex · doi:10.1016/j.cortex.2014.01.020 · Cited by 109
Self-citationThe Role of CA3 Hippocampal NMDA Receptors in Paired Associate Learning
Rajji, T. K., Chapman, D. E., Eichenbaum, H., & Greene, R. W. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4194-05.2006 · Cited by 108
Spatial View Cells in the Primate Hippocampus and Memory Recall
Rolls, E. T., & Xiang, J.-Z. (2006) · Reviews in the Neurosciences · doi:10.1515/revneuro.2006.17.1-2.175 · Cited by 108
Self-citationHippocampal–cortical interactions and the dynamics of memory trace reactivation
Schwindel, C. D., & McNaughton, B. L. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53839-0.00011-9 · Cited by 107
Stringer, S. M., Rolls, E. T., Trappenberg, T. P., & de Araújo, I. E. (2002) · Network Computation in Neural Systems · doi:10.1088/0954-898x_13_4_301 · Cited by 104
Self-citationEvaluating the temporal context of episodic memory: The role of CA3 and CA1
Hunsaker, M. R. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.11.015 · Cited by 101
Kesner, R. P., Hunsaker, M. R., & Warthen, M. W. (2008) · Behavioral Neuroscience · doi:10.1037/a0013592 · Cited by 100
(2008) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(08)x0003-7 · Cited by 98
Invariant Object Recognition in the Visual System with Novel Views of 3D Objects
Stringer, S. M., & Rolls, E. T. (2002) · Neural Computation · doi:10.1162/089976602760407982 · Cited by 97
Self-citationA unified model of spatial and episodic memory
Rolls, E. T., Stringer, S. M., & Trappenberg, T. P. (2002) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2009 · Cited by 97
Self-citationRole of long‐term synaptic modification in short‐term memory
Kesner, R. P., & Rolls, E. T. (2001) · Hippocampus · doi:10.1002/hipo.1040 · Cited by 95
Self-citationGenetic neuroscience of mammalian learning and memory
Tonegawa, S., Nakazawa, K., & Wilson, M. A. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1243 · Cited by 95
The CRISP theory of hippocampal function in episodic memory
Cheng, S. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00088 · Cited by 94
Long-Term Potentiation in Two Synaptic Systems of the Hippocampal Brain Slice
Brown, T. H., Ganong, A. H., Kairiss, E. W., Keenan, C. L., & Kelso, S. R. (1989) · Elsevier eBooks · doi:10.1016/b978-0-12-148955-7.50018-7 · Cited by 92
Simulation studies of the CA3 hippocampal subfield modelled as an attractor neural network
Rolls, E. T., Treves, A., Foster, D. J., & Pérez-Vicente, C. (1997) · Neural Networks · doi:10.1016/s0893-6080(97)00092-0 · Cited by 92
Self-citationRondi‐Reig, L., Libbey, M., Eichenbaum, H., & Tonegawa, S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.041620798 · Cited by 92
Miller, P. C., & Wang, X. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508072103 · Cited by 91
Neuronal selectivity, population sparseness, and ergodicity in the inferior temporal visual cortex
Franco, L., Rolls, E. T., Aggelopoulos, N. C., & Jerez, J. M. (2007) · Biological Cybernetics · doi:10.1007/s00422-007-0149-1 · Cited by 91
Self-citationRolls, E. T. (2009) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1 · Cited by 83
Self-citationIntrinsic connections of the macaque monkey hippocampal formation: II. CA3 connections
Kondo, H., Lavenex, P., & Amaral, D. G. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22056 · Cited by 80
Quantitative estimate of the information relayed by the Schaffer collaterals
Treves, A. (1995) · Journal of Computational Neuroscience · doi:10.1007/bf00961437 · Cited by 78
Memory for places: A navigational model in support of Marr's theory of hippocampal function
Recce, M. L., & Harris, K. D. (1996) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:6 · Cited by 78
Stringer, S. M., Rolls, E. T., & Trappenberg, T. P. (2003) · Neural Networks · doi:10.1016/s0893-6080(03)00210-7 · Cited by 71
Self-citationOn the design of neural networks in the brain by genetic evolution
Rolls, E. T., & Stringer, S. M. (2000) · Progress in Neurobiology · doi:10.1016/s0301-0082(99)00066-0 · Cited by 68
Self-citationFunctions of the primate hippocampus in spatial and nonspatial memory
Rolls, E. T. (1991) · Hippocampus · doi:10.1002/hipo.450010310 · Cited by 67
Self-citationde Araújo, I. E., Rolls, E. T., & Stringer, S. M. (2001) · Hippocampus · doi:10.1002/hipo.1085 · Cited by 67
Self-citationCortical plasticity: LTP and LTD
Sacktor, T. C. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01024-7 · Cited by 65
Heimer, L. (1995) · Springer eBooks · doi:10.1007/978-1-4612-2478-5_21 · Cited by 58
Self-organizing continuous attractor network models of hippocampal spatial view cells
Stringer, S. M., Rolls, E. T., & Trappenberg, T. P. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.08.003 · Cited by 57
Self-citationTheoretical and Neurophysiological Analysis of the Functions of the Primate Hippocampus in MemoryPreprint
Rolls, E. T. (1990) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1990.055.01.095 · Cited by 57
Self-citationHow Informative Are Spatial CA3 Representations Established by the Dentate Gyrus?
Cerasti, E., & Treves, A. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000759 · Cited by 56
Holding Multiple Items in Short Term Memory: A Neural Mechanism
Rolls, E. T., Dempere‐Marco, L., & Deco, G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061078 · Cited by 54
Self-citationSequential Memory: A Putative Neural and Synaptic Dynamical Mechanism
Deco, G., & Rolls, E. T. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/0898929053124875 · Cited by 54
Self-citationDaumas, S., Ceccom, J., Halley, H., Francès, B., & Lassalle, J. (2009) · Learning & Memory · doi:10.1101/lm.1418309 · Cited by 50
Spatial view cells in the hippocampus, and their idiothetic update based on place and head direction
Rolls, E. T., & Stringer, S. M. (2005) · Neural Networks · doi:10.1016/j.neunet.2005.08.006 · Cited by 46
Self-citationDilution and sparse coding in threshold-linear nets
Treves, A. (1991) · Journal of Physics A Mathematical and General · doi:10.1088/0305-4470/24/1/038 · Cited by 41
Selective temporal resections and spatial memory impairment: Cue dependent lateralization effects
Barkas, L. J., Henderson, J. L., Hamilton, D. A., Redhead, E. S., & Gray, W. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.035 · Cited by 39
Advantages of dilution in the connectivity of attractor networks in the brain
Rolls, E. T. (2012) · Biologically Inspired Cognitive Architectures · doi:10.1016/j.bica.2012.03.003 · Cited by 37
Self-citationFunctions of the primate hippocampus in spatial processing and memory
Rolls, E. T. (1991) · doi:10.1093/oso/9780198542841.003.0019 · Cited by 34
Self-citationCortical attractor network dynamics with diluted connectivity
Rolls, E. T., & Webb, T. J. (2011) · Brain Research · doi:10.1016/j.brainres.2011.08.002 · Cited by 31
Self-citationRecall of spatial patterns stored in a hippocampal slice by long-term potentiation
Jackson, M. B. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00533.2013 · Cited by 31
The spatial representations acquired in CA3 by self-organizing recurrent connections
Cerasti, E., & Treves, A. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00112 · Cited by 29
Pattern retrieval in threshold-linear associative nets
Simmen, M. W., Treves, A., & Rolls, E. T. (1996) · Network Computation in Neural Systems · doi:10.1080/0954898x.1996.11978657 · Cited by 24
Self-citationStringer, S. M., & Rolls, E. T. (2006) · Network Computation in Neural Systems · doi:10.1080/09548980601004032 · Cited by 24
Self-citationNoise in Attractor Networks in the Brain Produced by Graded Firing Rate Representations
Webb, T. J., Rolls, E. T., Deco, G., & Feng, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023630 · Cited by 20
Self-citationNeural dynamics of cross-modal and cross-temporal associations
Deco, G., Ledberg, A., Almeida, R., & Fuster, J. M. (2005) · Experimental Brain Research · doi:10.1007/s00221-005-2374-y · Cited by 18
Active Spatial Information Processing in the Septo-Hippocampal System
Ono, T., & Nishijo, H. (1999) · Hippocampus · doi:10.1002/(sici)1098-1063(1999)9:4 · Cited by 17
Self-citationUnveiling the metric structure of internal representations of space
Stella, F., Cerasti, E., & Treves, A. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00081 · Cited by 16
Kesner, R. P., Morris, A. M., & Weeden, C. S. S. (2012) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780195392661.013.0018 · Cited by 15
Walters, D., Stringer, S. M., & Rolls, E. T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058330 · Cited by 13
Self-citationCortico-hippocampal communication by way of parallel parahippocampal-subicular pathways.
Lavenex (2000) · Pure Amsterdam UMC · doi:10.1002/1098-1063(2000)10:4 · Cited by 1
- Self-citation
Flagged first, then by citations
6 of the 191 references couldn’t be matched to a known paper.
Research works printed but not linked: 7
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- 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
- 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
- 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
- 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
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Frost, R., Armstrong, B. C., Siegelman, N., & Christiansen, M. H. (2015) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2014.12.010 · Cited by 601
Limbic systems for emotion and for memory, but no single limbic system
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Self-citationHow Can Hearing Loss Cause Dementia?
Griffiths, T. D., Lad, M., Kumar, S., Holmes, E., McMurray, B., Maguire, E. A., Billig, A. J., & Sedley, W. (2020) · Neuron · doi:10.1016/j.neuron.2020.08.003 · Cited by 389
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Metadata
- 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)
- 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
- gold
- doi.org
- 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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