A computational theory of hippocampal function, and tests of the theory: New developments
Abstract
The aims of the paper are to update Rolls' quantitative computational theory of hippocampal function and the predictions it makes about the different subregions (dentate gyrus, CA3 and CA1), and to examine behavioral and electrophysiological data that address the functions of the hippocampus and particularly its subregions. Based on the computational proposal that the dentate gyrus produces sparse representations by competitive learning and via the mossy fiber pathway forces new representations on the CA3 during learning (encoding), it has been shown behaviorally that the dentate gyrus supports spatial pattern separation during learning. Based on the computational proposal that CA3-CA3 autoassociative networks are important for episodic memory, it has been shown behaviorally that the CA3 supports spatial rapid one-trial learning, learning of arbitrary associations where space is a component, pattern completion, spatial short-term memory, and spatial sequence learning by associations formed between successive items. The concept that the CA1 recodes information from CA3 and sets up associatively learned backprojections to neocortex to allow subsequent retrieval of information to neocortex, is consistent with findings on consolidation. Behaviorally, the CA1 is implicated in processing temporal information as shown by investigations requiring temporal order pattern separation and associations across time; and computationally this could involve associations in CA1 between object and timing information that have their origins in the lateral and medial entorhinal cortex respectively. The perforant path input from the entorhinal cortex to DG is implicated in learning, to CA3 in retrieval from CA3, and to CA1 in retrieval after longer time intervals ("intermediate-term memory") and in the temporal sequence memory for objects.
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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 [79]
According to mechanistic models of hippocampal memory function, the hippocampal neural network can shift between encoding and retrieval modes depending on the novelty degree of incoming spatial information.
“Thus, according to the mechanistic models of hippocampal memory function, the hippocampal neural network can shift between two functional modes, encoding and retrieval, depending on the novelty degree of the incoming spatial information [77,78,79].”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [79]
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 [79]
In mammals, allocentric navigation involves an extended cortico-hippocampal network that conveys highly processed visual and multisensory information to hippocampal circuits for transformation into 'world-centered' relational spatial representations.
“In mammals, allocentric navigation is thought to involve the operation of an extended cortico-hippocampal network that conveys highly processed visual and multisensory information to the hippocampal circuits for further processing and transformation into “world-centered” relational spatial representations [74,76,79,188,189,190,191,192].”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [79]
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 [79]
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- Authors
- Kesner, R. P., & Rolls, E. T.
- Affiliations
- University of Utah (US)
- University of Warwick (GB)
- Corresponding author
- Rolls, Edmund T.
- ORCID
- Rolls, Edmund T.
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2015-01
- Volume
- 48
- Pages
- 92-147
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2028346421
- Cited by
- 347
- References
- 28
- Citations by year
- 2026: 21 · 2025: 29 · 2024: 29 · 2023: 25 · 2022: 24 · 2021: 37 · 2020: 21 · 2019: 34 · 2018: 31 · 2017: 41 · 2016: 33 · 2015: 21 · 2014: 1
- FWCI
- 3.09
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Medical Research Council
- Human Frontier Science
- EEC BRAIN
- MRC Oxford Interdisciplinary Research Centre in Cognitive Neuroscience
- Oxford McDonnell-Pew Centre in Cognitive Neuroscience
- Oxford Centre for Computational Neuroscience
- NSF (IBN-0135273)
- NIH (5R01MH065314-02)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampal function, roll, dentate gyrus, CA3, CA1, sparse representation, competitive learning, mossy fiber pathway, pattern separation, pattern completion, episodic memory, autoassociative networks, spatial learning, one-trial learning, spatial short-term memory, sequence learning, memory consolidation, temporal order, entorhinal cortex, perforant path, intermediate-term memory, temporal sequence memory, memory retrieval
- MeSH terms
- Animals, Computer Simulation, Hippocampus, Humans, Memory, Models, Neurological, Neurons, Space Perception
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