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Pattern separation, completion, and categorisation in the hippocampus and neocortex
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 and also a large number of independent memories stored in CA3 include: a sparse distributed representation, representations that are independent due to the randomizing effect of the mossy fibres, 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, and in the dentate to CA3 connections that have diluted connectivity. 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. New results on competitive networks show which factors contribute to their ability to perform pattern separation, pattern clustering, and pattern categorisation, and how these apply in different hippocampal and neocortical systems.
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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 [81]
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Georges‐François, P. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.3.197 · Cited by 227
Lassalle, J., Bataille, T., & Halley, H. (2000) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3931 · Cited by 216
Goodrich‐Hunsaker, N. J., Hunsaker, M. R., & Kesner, R. P. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.1.16 · Cited by 208
Rolls, E. T., & Treves, A. (1990) · Network Computation in Neural Systems · doi:10.1088/0954-898x_1_4_002 · Cited by 208
Self-citationMemory, Attention, and Decision-Making: A unifying computational neuroscience approach
Rolls, E. T. (2007) · Cited by 205
Self-citationA Unified Mathematical Framework for Coding Time, Space, and Sequences in the Hippocampal Region
Howard, M. W., MacDonald, C. J., Tiganj, Z., Shankar, K. H., Du, Q., Hasselmo, M. E., & Eichenbaum, H. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5808-12.2014 · Cited by 203
The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat
Gold, A., & Kesner, R. P. (2005) · Hippocampus · doi:10.1002/hipo.20103 · Cited by 196
Brain mechanisms for perceptual and reward-related decision-making
Deco, G., Rolls, E. T., Albantakis, L., & Romo, R. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.01.010 · Cited by 196
Self-citationBattaglia, F. P., & Treves, A. (1998) · Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics · doi:10.1103/physreve.58.7738 · Cited by 194
Stefanacci, L., SUZUKI, W. A., & Amaral, D. G. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961125)375:4 · Cited by 192
Stringer, S. M., Trappenberg, T. P., Rolls, E. T., & de Araújo, I. E. (2002) · Network Computation in Neural Systems · doi:10.1088/0954-898x/13/2/304 · Cited by 191
Self-citationAttention and working memory: a dynamical model of neuronal activity in the prefrontal cortex
Deco, G., & Rolls, E. T. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02956.x · Cited by 189
Self-citationCerebral cortex : principles of operation
Rolls, E. T. (2016) · doi:10.82444/warw.33712699 · Cited by 187
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
A model of episodic memory: Mental time travel along encoded trajectories using grid cells
Hasselmo, M. E. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.07.005 · Cited by 166
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
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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-citationMemory Deficits Characterized by Patterns of Lesions to the Hippocampus and Parahippocampal Cortex
Bohbot, V. D., Allen, J. J. B., & Nadel, L. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06737.x · Cited by 144
Neural models of plasticity: experimental and theoretical approaches
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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-citationAn assessment of Marr’s theory of the hippocampus as a temporary memory store
Willshaw, D. J., & Buckingham, J. T. (1990) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1990.0165 · Cited by 130
Associative memory: A system-theoretical approach
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The recall of events through the learning of associations between their parts
Gardner-Medwin, A. R. (1976) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1976.0084 · Cited by 125
A 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-citationThe neural and molecular bases of learning
Bruyn, G. W. (1987) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(87)90195-x · Cited by 123
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The Noisy Brain: Stochastic Dynamics as a Principle of Brain Function
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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
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-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
Hippocampal–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
Information Theory and the Brain
Baddeley, R. (2000) · Cambridge University Press eBooks · doi:10.1017/cbo9780511665516 · Cited by 93
Computational Models of Learning in Simple Neural Systems
(1989) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/s0079-7421(08)x6009-8 · Cited by 93
Long-Term Potentiation in Two Synaptic Systems of the Hippocampal Brain Slice
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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-citationOpen Peer Review by a Selected-Papers Network
Lee, C. J. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00001 · Cited by 85
Rolls, 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
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-citationSelf-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-citation
Flagged first, then by citations
4 of the 227 references couldn’t be matched to a known paper.
Research works printed but not linked: 3
- McNaughton, 1991, Associative pattern completion in hippocampal circuits: New evidence and new questions, Brain Research Reviews, 16, 193
- Rolls, 1995, A model of the operation of the hippocampus and entorhinal cortex in memory, International Journal of Neural Systems, 6, 51
- Witter, 2000, Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways, Hippocampus, 10, 398, 10.1002/1098-1063(2000)10:4<398::aid-hipo6>3.0.co;2-k · DOI
Cited by
Sorted by citations
Roddy, D. W., Farrell, C., Doolin, K., Roman, E., Tozzi, L., Frodl, T., O’Keane, V., & O’Hanlon, E. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.08.021 · Cited by 287
The enigmatic mossy cell of the dentate gyrus
Scharfman, H. E. (2016) · Nature reviews. Neuroscience · doi:10.1038/nrn.2016.87 · Cited by 281
Re-evaluating Circuit Mechanisms Underlying Pattern Separation
Cayco-Gajic, N. A., & Silver, R. A. (2019) · Neuron · doi:10.1016/j.neuron.2019.01.044 · Cited by 234
“As the first stage in this pathway, the dentate gyrus is thought to separate entorhinal input patterns prior to memory storage in the hippocampus (Marr, 1971; McNaughton and Morris, 1987; Yassa and Stark, 2011; Schmidt et al., 2012; Knierim and Neunuebel, 2016; Rolls, 2016).”
Cerebral cortex : principles of operation
Rolls, E. T. (2016) · doi:10.82444/warw.33712699 · Cited by 187
Self-citationThe storage and recall of memories in the hippocampo-cortical system
Rolls, E. T. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2744-3 · Cited by 195
“For recall, the hippocampal output can be thought of as a pointer to neocortical neurons via which memories can be called by using the backprojection pathways (Kesner and Rolls 2015; Rolls 2016a).”
BackgroundMethodResultInfluentialSelf-citation
Metadata
- Authors
- Rolls, E. T.
- Affiliations
- University of Warwick (GB)
- Corresponding author
- Rolls, Edmund T.
- ORCID
- Rolls, Edmund T.
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 129
- Pages
- 4-28
- ISSN
- 1074-7427 (ISSN-L)
- OpenAlex
- W889908523
- Semantic Scholar
- dee8fed2414a8b21d9bf5724732f82ca2356190b
- Cited by
- 234
- References
- 227
- Citations by year
- 2026: 28 · 2025: 25 · 2024: 29 · 2023: 24 · 2022: 19 · 2021: 29 · 2020: 18 · 2019: 21 · 2018: 17 · 2017: 15 · 2016: 9
- FWCI
- 8.22
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurobiology of Learning and Memory (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Medical Research Council
- Human Frontier Science Program
- EEC BRAIN
- MRC Oxford Interdisciplinary Research Centre in Cognitive Neuroscience
- Oxford McDonnell-Pew Centre in Cognitive Neuroscience
- Oxford Centre for Computational Neuroscience
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- pattern separation, pattern completion, hippocampus, CA3, dentate gyrus, neocortex, attractor networks, sparse distributed representations, mossy fibers, long-term potentiation, perforant path, entorhinal cortex, place cells, grid cells, competitive learning, pattern generalization, memory retrieval
- MeSH terms
- Animals, Association Learning, Humans, Models, Neurological, Neural Pathways, Neurons, Mental Recall, Synapses, Neocortex, Pattern Recognition, Physiological, CA3 Region, Hippocampal
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