Hippocampus, Retrosplenial and Parahippocampal Cortices Encode Multicompartment 3D Space in a Hierarchical Manner
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Abstract
Humans commonly operate within 3D environments such as multifloor buildings and yet there is a surprising dearth of studies that have examined how these spaces are represented in the brain. Here, we had participants learn the locations of paintings within a virtual multilevel gallery building and then used behavioral tests and fMRI repetition suppression analyses to investigate how this 3D multicompartment space was represented, and whether there was a bias in encoding vertical and horizontal information. We found faster response times for within-room egocentric spatial judgments and behavioral priming effects of visiting the same room, providing evidence for a compartmentalized representation of space. At the neural level, we observed a hierarchical encoding of 3D spatial information, with left anterior hippocampus representing local information within a room, while retrosplenial cortex, parahippocampal cortex, and posterior hippocampus represented room information within the wider building. Of note, both our behavioral and neural findings showed that vertical and horizontal location information was similarly encoded, suggesting an isotropic representation of 3D space even in the context of a multicompartment environment. These findings provide much-needed information about how the human brain supports spatial memory and navigation in buildings with numerous levels and rooms.
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It has been observed that people do not always rely on a coherent Euclidean map for navigation.
“However, it has been observed that people do not always rely on a coherent Euclidean map for navigation.”
From Cognitive Maps for a Non-Euclidean Environment: Path Integration and Spatial Memory on a Sphere (2024) · cites this paper as Kim & Maguire, 2018
Real-world spaces are segmented by physical barriers that yield various substructures or regions.
“Real-world spaces are segmented by physical barriers that yield various substructures or regions 41,[130][131][132][133] .”
From From cognitive maps to spatial schemas (2023) · cites this paper as [130]
fMRI repetition suppression effects in several brain regions, including the RSC, HPC and PHC, in participants navigating to target landmarks in rooms within a virtual multi-level building revealed that the repetition suppression effect was similar across rooms that had the same layout, suggesting generalization of neural representations.
“fMRI repetition suppression [G] effects in several brain regions, including the RSC, HPC and PHC in participants navigating to target landmarks in rooms within a virtual multi-level building revealed that the repetition suppression effect was similar across rooms that had the same layout, suggesting generalization of neural representations 130 .”
From From cognitive maps to spatial schemas (2023) · cites this paper as [130]
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- Authors
- Kim, M., & Maguire, E. A.
- Affiliations
- Wellcome Centre for Human Neuroimaging, Institute of Neurology, University College London, London WC1N 3AR, UK
- Wellcome Centre for Human Neuroimaging (GB)
- Corresponding author
- Maguire, Eleanor A
- ORCID
- Maguire, Eleanor A
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2018-03-15
- Volume
- 28
- Issue
- 5
- Pages
- 1898-1909
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- PMC
- PMC5907342
- OpenAlex
- W2949496141
- Cited by
- 45
- References
- 62
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 7 · 2023: 5 · 2022: 4 · 2021: 7 · 2020: 6 · 2019: 5 · 2018: 1
- FWCI
- 2.52
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cerebral Cortex (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (101759/Z/13/Z, 203147/Z/16/Z, 102263/Z/13/Z)
- Samsung PhD Studentship
- Topics
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- three-dimensional representation, hippocampus, retrosplenial cortex, parahippocampal cortex, spatial memory, repetition suppression, virtual worlds
- MeSH terms
- Egocentrism, Adolescent, Adult, Analysis of Variance, Female, Hippocampus, Humans, Judgment, Magnetic Resonance Imaging, Male, Memory, Neural Pathways, Oxygen, Social Dominance, Space Perception, User-Computer Interface, Parahippocampal Gyrus, Imaging, Three-Dimensional, Young Adult
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