A critical review of the allocentric spatial representation and its neural underpinnings: toward a network-based perspective

Ekstrom, Arne D.; Arnold, Aiden E. G. F.; Iaria, Giuseppe

doi:10.3389/fnhum.2014.00803

Cited by 263Spatial Cognition and NavigationMemory and Neural MechanismsMemory Processes and Influences

A critical review of the allocentric spatial representation and its neural underpinnings: toward a network-based perspective

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Ekstrom, Arne D., Arnold, Aiden E. G. F., Iaria, Giuseppe·2014·Frontiers in Human Neuroscience

DOI 10.3389/fnhum.2014.00803PMC PMC4193251

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Abstract

While the widely studied allocentric spatial representation holds a special status in neuroscience research, its exact nature and neural underpinnings continue to be the topic of debate, particularly in humans. Here, based on a review of human behavioral research, we argue that allocentric representations do not provide the kind of map-like, metric representation one might expect based on past theoretical work. Instead, we suggest that almost all tasks used in past studies involve a combination of egocentric and allocentric representation, complicating both the investigation of the cognitive basis of an allocentric representation and the task of identifying a brain region specifically dedicated to it. Indeed, as we discuss in detail, past studies suggest numerous brain regions important to allocentric spatial memory in addition to the hippocampus, including parahippocampal, retrosplenial, and prefrontal cortices. We thus argue that although allocentric computations will often require the hippocampus, particularly those involving extracting details across temporally specific routes, the hippocampus is not necessary for all allocentric computations. We instead suggest that a non-aggregate network process involving multiple interacting brain areas, including hippocampus and extra-hippocampal areas such as parahippocampal, retrosplenial, prefrontal, and parietal cortices, better characterizes the neural basis of spatial representation during navigation. According to this model, an allocentric representation does not emerge from the computations of a single brain region (i.e., hippocampus) nor is it readily decomposable into additive computations performed by separate brain regions. Instead, an allocentric representation emerges from computations partially shared across numerous interacting brain regions. We discuss our non-aggregate network model in light of existing data and provide several key predictions for future experiments.

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Spatial navigation is influenced by several factors such as age and individual spatial abilities.
“This finding aligns with the notion that spatial navigation is influenced by several factors such as age and individual spatial abilities11,12,36–38.”
From Long-term Memory Reorganization of Navigational Episodes (2026) · cites this paper as [11]
The section on allocentric representation as a network phenomenon reports that network efficiency predicted participants’ accuracy in orienting within a virtual city, supporting variation in individual spatial ability. The passages found do not address age as a factor in navigation (searched: age, aging, age-related). No page numbers are available in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Memory of egocentric and allocentric representational modes relies on at least partially dissociable neural substrates.
“Studies suggest that memory of these representational modes relies on at least partially dissociable neural substrates5,11,12.”
From Long-term Memory Reorganization of Navigational Episodes (2026) · cites this paper as [11]

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Authors: Ekstrom, A. D., Arnold, A. E. G. F., & Iaria, G.
Affiliations: University of California, Davis (US)
University of Calgary (CA)
Corresponding author: Ekstrom, Arne D.
ORCID: Ekstrom, Arne D.
Arnold, Aiden E. G. F.
Iaria, Giuseppe
Venue: Frontiers in Human Neuroscience
Publisher: Frontiers Media SA
Published: 2014-10-10
Volume: 8
Pages: 803-803
ISSN: 1662-5161 (ISSN-L)
DOI: 10.3389/fnhum.2014.00803
PMC: PMC4193251
OpenAlex: W2120207633
Cited by: 263
References: 138
Citations by year: 2026: 22 · 2025: 27 · 2024: 15 · 2023: 22 · 2022: 19 · 2021: 29 · 2020: 28 · 2019: 17 · 2018: 31 · 2017: 26 · 2016: 12 · 2015: 14 · 2013: 1
FWCI: 3.95
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Human Neuroscience (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
eScholarship (California Digital Library) (submittedVersion)
Funders: Alfred P. Sloan Foundation
National Institutes of Health
Natural Sciences and Engineering Research Council of Canada (RT735872)
National Institute of Neurological Disorders and Stroke (R01NS076856)
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: allocentric spatial representation, spatial memory, hippocampus, parahippocampal cortex, retrosplenial cortex, prefrontal cortex, parietal cortex, egocentric representation, neural network model, navigation, metric representation, brain region interactions

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A critical review of the allocentric spatial representation and its neural underpinnings: toward a network-based perspective

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