Space in the brain: How the hippocampal formation supports spatial cognition
Open accessAbstract
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 teleost spatial strategies necessarily involve complex learning and memory capabilities and require flexible representational mechanisms, the most remarkable of which is allocentric navigation based on map-like spatial memory.
“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]
The Introduction (page unavailable) describes allocentric representations as a basis for cognitive maps and long-term memory of spatial relationships and routes. It does not address teleosts or establish that their spatial strategies necessarily require complex learning and flexible representational mechanisms. (LLM, conf=0.86)
Experimental — accuracy not yet measuredSuch hypothetical memory representations presumably encode the spatial relationships between all known places and landmarks in a common allocentric reference frame or unitary global map, accessible as a whole, and can operate to infer spatial relationships between any represented elements.
“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]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredThe hippocampus of tetrapods is 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.
“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]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredThe medial pallium or hippocampus of land vertebrates plays a central role in allocentric spatial navigation.
“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]
The Introduction describes an allocentric spatial system centred on the hippocampus, and the human spatial cognition section says the hippocampus particularly supports allocentric spatial memory. The paper discusses evidence from rodents, primates and humans, but the cited passages do not establish the claim for land vertebrates generally or identify the medial pallium as playing that role. Page numbers are unavailable in our copy. (LLM, conf=0.83)
Experimental — accuracy not yet measuredHippocampal lesions in mammals, birds, and reptiles produce impairments on spatial tasks that require the use of map-like or relational spatial memory.
“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]
The Human spatial cognition section reports that hippocampal damage accompanies deficits in spatial orientation and navigation and that the hippocampus supports allocentric spatial memory. The References also list a study of impaired place navigation in rats with hippocampal lesions. Our copy does not establish the claimed lesion-related impairments in birds or reptiles. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Mammalian extra-hippocampal cortical areas contain functionally specialized neurons such as head direction cells, border cells, and grid cells that likely encode relevant spatial information in egocentric coordinates.
“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]
The Head Direction Cells and Grid Cells sections identify specialized spatial neurons, and the Boundary Cells section places boundary cells outside the hippocampus proper. But the paper does not describe these cell types as encoding space in egocentric coordinates: the Head Direction Cells section explicitly calls their heading signal allocentric, while the Introduction associates egocentric coding with other cortical neurons, notably in parietal cortex. Several of the named cell types are also described as belonging to the hippocampal formation, rather than being wholly outside it (page numbers unavailable). (LLM, conf=0.89)
Experimental — accuracy not yet measuredTolerance to partial losses of spatial information has been proposed to be a key characteristic of mammalian hippocampus-dependent map-like spatial memory.
“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]
Place cells, hippocampal neurons that fire when the animal occupies a particular location, are proposed as the higher instance of a brain system that builds map-like spatial memory representations anchored in the external world, contributing to allocentric navigation.
“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]
The dorsolateral telencephalon of teleost fish is a critical brain center for allocentric navigation based on map-like spatial memory.
“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]
The Introduction describes allocentric, map-like spatial representations in the hippocampal formation, and the section on human spatial cognition discusses allocentric memory in humans. Neither addresses the dorsolateral telencephalon of teleost fish or its role in navigation; searches for “teleost,” “dorsolateral telencephalon,” and fish spatial learning found no passage on that claim. The cited passages have no page numbers in our copy. (LLM, conf=0.75)
Experimental — accuracy not yet measured
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Self-citationWhat can the hippocampal representation of environmental geometry tell us about Hebbian learning?
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Hidden state inference requires abstract contextual representations in the ventral hippocampus
Mishchanchuk, K., Gregoriou, G. C., Qü, A. J., Kastler, A., Huys, Q. J. M., Wilbrecht, L., & MacAskill, A. F. (2024) · Science · doi:10.1126/science.adq5874 · Cited by 51 · see citing works
Luppi, P., Billwiller, F., & Fort, P. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.03.002 · Cited by 50 · see citing works
- 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
- Physical Sciences › Engineering › Automotive Engineering › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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