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Space in the brain: how the hippocampal formation supports spatial cognition
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Over the past four decades, research has revealed that cells in the hippocampal formation provide an exquisitely detailed representation of an animal's current location and heading. These findings have provided the foundations for a growing understanding of the mechanisms of spatial cognition in mammals, including humans. We describe the key properties of the major categories of spatial cells: place cells, head direction cells, grid cells and boundary cells, each of which has a characteristic firing pattern that encodes spatial parameters relating to the animal's current position and orientation. These properties also include the theta oscillation, which appears to play a functional role in the representation and processing of spatial information. Reviewing recent work, we identify some themes of current research and introduce approaches to computational modelling that have helped to bridge the different levels of description at which these mechanisms have been investigated. These range from the level of molecular biology and genetics to the behaviour and brain activity of entire organisms. We argue that the neuroscience of spatial cognition is emerging as an exceptionally integrative field which provides an ideal test-bed for theories linking neural coding, learning, memory and cognition.
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“Some of these spatial strategies necessarily involve complex learning and memory capabilities and require the concurrence of flexible representational mechanisms, the most remarkable of which probably is allocentric navigation based on map-like spatial memory”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [72]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“Such hypothetical memory representations presumably encode the spatial relationships between all the known places and landmarks in a common allocentric reference frame or unitary global map, accessible as a whole, and that can operate to infer the spatial relationships between any of the represented elements.”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [72]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“The hippocampus of tetrapods seems to be essential in tasks requiring the formation of a memory of the spatial relationships of multiple elements and cues of the environment and those demanding the flexible expression of previously acquired spatial knowledge [72,73,75,76].”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [72]
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“A considerable amount of evidence shows that the medial pallium or hippocampus of land vertebrates plays a central role in allocentric spatial navigation.”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [72]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
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“For example, in mammals [39,57,72,149], birds [97,98,99,150,151,152,153], and reptiles [112,154,155,156,157], the hippocampal lesions produce impairments on spatial tasks that require the use of map-like or relational spatial memory.”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [72]
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“Mammalian extra-hippocampal cortical areas contain a variety of functionally specialized neurons with presumably distinct roles in the representation of space, i.e., “head direction cells”, “border cells”, and “grid cells”, that likely encode relevant spatial information in egocentric coordinates [72,193,194,195,196].”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [72]
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“The tolerance to partial losses of spatial information has been proposed to be a key characteristic of the mammalian hippocampus-dependent map-like spatial memory”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [72]
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“The “place cells”, i.e., hippocampal neurons that fire when the animal occupies a particular location of the space, have been proposed to be the higher instance of a brain system that builds up map-like spatial memory representations anchored in the external world, contributing to the neural computations required for allocentric navigation [39,72,74,197,198].”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [72]
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“These results closely resemble those obtained after hippocampus lesions in mammals, birds, and reptiles [39,57,72,97,98,112,152,157] and demonstrated that the dorsolateral telencephalon of teleost fish is a critical brain center for allocentric navigation based in map-like spatial memory.”
From Spatial Cognition in Teleost Fish: Strategies and Mechanisms (2021) · cites this paper as [72]
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Metadata
- Authors
- Hartley, T., Lever, C., Burgess, N., & O'Keefe, J.
- Affiliations
- University of York (GB)
- Durham University (GB)
- UCL Queen Square Institute of Neurology (GB)
- Sainsbury Wellcome Centre (GB)
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2014-02-05
- Volume
- 369
- Issue
- 1635
- Pages
- 20120510
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC3866435
- OpenAlex
- W2146561158
- Cited by
- 495
- References
- 219
- Citations by year
- 2026: 23 · 2025: 43 · 2024: 32 · 2023: 30 · 2022: 41 · 2021: 45 · 2020: 41 · 2019: 44 · 2018: 38 · 2017: 56 · 2016: 42 · 2015: 45 · 2014: 15
- FWCI
- 2.90
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Durham Research Online (Durham University) (submittedVersion, cc-by)
- Funders
- Wellcome Trust (095811)
- Medical Research Council
- Biotechnology and Biological Sciences Research Council (BB/G01342X/2, BB/G01342X/1)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- hippocampal formation, spatial cognition, place cells, head direction cells, grid cells, boundary cells, theta oscillations, spatial representation, neural coding, computational modelling, memory, learning
- MeSH terms
- Action Potentials, Animals, Cognition, Computer Simulation, Hippocampus, Humans, Models, Neurological, Neurons, Space Perception, Theta Rhythm, Mice, Rats
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