Cited by 393Memory and Neural MechanismsMemory Processes and InfluencesSpatial Cognition and Navigation

The DOI matches its Crossref record; 75 of the 75 references it cites were found in a registry or an index; none of the 61 sources its claims cite is checked for support yet.

The hippocampus: a manifesto for change

Open access
Maguire, Eleanor A., Mullally, Sinéad L.·2013·Journal of Experimental Psychology: General

Abstract

We currently lack a unified and mechanistic account of how the hippocampus supports a range of disparate cognitive functions that includes episodic memory, imagining the future, and spatial navigation. Here, we argue that in order to leverage this long-standing issue, traditional notions regarding the architecture of memory should be eschewed. Instead, we invoke the idea that scenes are central to hippocampal information processing. This view is motivated by mounting evidence that the hippocampus is constantly constructing spatially coherent scenes, automatically anticipating and synthesizing representations of the world beyond the immediate sensorium. By characterizing the precise relationship between scenes and the hippocampus, we believe a theoretically enriched understanding of its fundamental role and its breakdown in pathology can emerge.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

Maguire argues that the hippocampus is not primarily an episodic memory device but instead automatically constructs spatially coherent scenes, a view termed scene construction theory (SCT). This framework is proposed to unify episodic memory, future imagining, spatial navigation, and related functions, with boundary extension and fMRI evidence cited as key support.

Key findings

  • SCT posits that scenes are the “primary currency” of the hippocampus: it constructs atemporal, spatially coherent scenes that provide the backdrop for episodic memories, imagined future experiences, spatial navigation, and perhaps mind wandering and dreaming.
  • In Mullally, Intraub, and Maguire (2012), seven patients with selective bilateral hippocampal damage and amnesia showed more veridical memory and significantly fewer boundary-extension errors than controls across three independent measures; in the haptic task, patients’ reconstructed scene areas did not differ significantly from studied scenes, whereas controls’ reconstructed scenes were significantly larger.
  • In a scene probe task, these patients could recount expected beyond-view details conceptually but produced significantly fewer spatial details than controls and typically reported being unable to visualize the extended scene in their mind’s eye.
  • Chadwick, Mullally, and Maguire (in press) found that boundary extension in healthy controls was associated with hippocampus and parahippocampal cortex engagement, with the hippocampus exerting top-down influence on PHC and early visual cortex; patient P01, densely amnesic but with preserved scene construction, engaged remnant right hippocampus during scene construction.

Methods

  • Theoretical manifesto/review, not an empirical study; the authors synthesize neuropsychological and neuroimaging findings to propose SCT and compare it with alternative accounts such as relational memory, constructive episodic simulation, and cognitive map/boundary vector cell models.
  • Evidence discussed includes prior studies of patients with bilateral hippocampal lesions/amnesia, including seven patients in Mullally et al. (2012) and patient P01, plus fMRI studies in healthy participants and P01.
  • Main analysis is conceptual: the paper argues that scene construction, rather than memory or time, is the common hippocampal process underlying disparate functions.

Limitations

  • The authors state their proposal is “not bulletproof” and requires a good deal more investigation; the piece is not intended as a forensic comparison of hippocampal theories or an exhaustive literature review.
  • The authors state further work is needed to elucidate boundary extension in patients with lesions outside the hippocampus, to uncover exactly how the hippocampus facilitates scene construction, to examine its relationship with pattern separation and pattern completion, and to definitively establish that an inability to construct scenes explains the full constellation of deficits from hippocampal pathology.
  • The text makes evident that no new primary data are reported and that some proposals are speculative, such as the suggestion that verbal memory tasks may benefit from scene-based imagery strategies; SCT could be falsified by a patient with impaired scene construction and preserved episodic memory, which has not yet been identified.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1037/a0033650

Cites

75 of 75 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Figures

Figure 1 Examples of imagined scenarios. The cue is shown at the top, below which is an excerpt from P03, a patient with bilateral hippocampal damage, followed by that of a matched control participant. Reprinted from “Patients With Hippocampal Amnesia Cannot Imagine New Experiences,” by D. Hassabis, D. Kumaran, S. D. Vann, and E. A. Maguire, 2007, Proceedings of the National Academy of Sciences of the United States of America, 104, p. 1727. Copyright 2007 by the National Academy of Sciences.
Figure 1 Examples of imagined scenarios. The cue is shown at the top, below which is an excerpt from P03, a patient with bilateral hippocampal damage, followed by that of a matched control participant. Reprinted from “Patients With Hippocampal Amnesia Cannot Imagine New Experiences,” by D. Hassabis, D. Kumaran, S. D. Vann, and E. A. Maguire, 2007, Proceedings of the National Academy of Sciences of the United States of America, 104, p. 1727. Copyright 2007 by the National Academy of Sciences.CC BY · PubMed Central
Figure 2 Scene construction theory contends that episodic memory, navigation, imagining fictitious scenes, and imagining the future encompass many processes that are not the primary concern of the hippocampus. Nevertheless, it proposes that they each rely on the hippocampus for a critical component, which is the construction of spatially coherent scenes.
Figure 2 Scene construction theory contends that episodic memory, navigation, imagining fictitious scenes, and imagining the future encompass many processes that are not the primary concern of the hippocampus. Nevertheless, it proposes that they each rely on the hippocampus for a critical component, which is the construction of spatially coherent scenes.CC BY · PubMed Central
Figure 3 The phenomenon of boundary extension (BE). When we see a picture of a scene (top panel), we automatically extrapolate beyond the physical edges of that scene (second panel). This active extension of the scene is the “BE effect” (Phase 1). In Phase 2, when exactly the same picture is presented at test (fourth panel), we compare the now-extended internal representation of the original scene (third panel) to the test picture, leading to the impression that the test picture is “closer” than the original study picture, even though they are identical. This memory error is the “BE error.” From “The Hippocampus Extrapolates Beyond the View in Scenes: An fMRI Study of Boundary Extension,” By M. J. Chadwick, S. L. Mullally, and E. A. Maguire, in press, Cortex. Copyright by Elsevier. Reprinted with permission.
Figure 3 The phenomenon of boundary extension (BE). When we see a picture of a scene (top panel), we automatically extrapolate beyond the physical edges of that scene (second panel). This active extension of the scene is the “BE effect” (Phase 1). In Phase 2, when exactly the same picture is presented at test (fourth panel), we compare the now-extended internal representation of the original scene (third panel) to the test picture, leading to the impression that the test picture is “closer” than the original study picture, even though they are identical. This memory error is the “BE error.” From “The Hippocampus Extrapolates Beyond the View in Scenes: An fMRI Study of Boundary Extension,” By M. J. Chadwick, S. L. Mullally, and E. A. Maguire, in press, Cortex. Copyright by Elsevier. Reprinted with permission.CC BY · PubMed Central
Figure 4 Rapid serial visual presentation boundary extension (BE) task. (a) Timeline of an example trial. After viewing two consecutively presented identical scenes, participants rated the perspective of the second scene relative to the first (as “closer-up,” “the same,” or “farther away”). (b) BE is revealed by a disproportionally large number of erroneous “closer-up” responses, which were greater for the controls than the hippocampal amnesic patients, who made significantly more accurate (“the same”) responses. (c) The control participants were significantly more confident when making their erroneous “closer-up” responses, whereas the patients were significantly more confident when making their correct “the same” responses. Means (±SEM). Q1 = Question 1; Q2 = Question 2. * p < .05. From “Attenuated Boundary Extension Produces a Paradoxical Memory Advantage in Amnesic Patients,” by S. L. Mullally, H. Intraub, and E. A. Maguire, 2012, Current Biology, 22, p. 263. Copyright 2012 by Elsevier. Reprinted with permission.
Figure 4 Rapid serial visual presentation boundary extension (BE) task. (a) Timeline of an example trial. After viewing two consecutively presented identical scenes, participants rated the perspective of the second scene relative to the first (as “closer-up,” “the same,” or “farther away”). (b) BE is revealed by a disproportionally large number of erroneous “closer-up” responses, which were greater for the controls than the hippocampal amnesic patients, who made significantly more accurate (“the same”) responses. (c) The control participants were significantly more confident when making their erroneous “closer-up” responses, whereas the patients were significantly more confident when making their correct “the same” responses. Means (±SEM). Q1 = Question 1; Q2 = Question 2. * p < .05. From “Attenuated Boundary Extension Produces a Paradoxical Memory Advantage in Amnesic Patients,” by S. L. Mullally, H. Intraub, and E. A. Maguire, 2012, Current Biology, 22, p. 263. Copyright 2012 by Elsevier. Reprinted with permission.CC BY · PubMed Central
Figure 5 A drawing boundary extension (BE) task. The left panel shows two example scene stimuli that were studied for 15 s and immediately drawn from memory. The example control participants (middle and right panels) drew a more extended expanse of background than was present in the original stimuli (demonstrating BE). By contrast, the example patient’s drawings (left panel) are more accurate, showing a paradoxically better memory for the studied scenes. Reprinted from “Attenuated Boundary Extension Produces a Paradoxical Memory Advantage in Amnesic Patients,” by S. L. Mullally, H. Intraub, and E. A. Maguire, 2012, Current Biology, 22, p. 264. Copyright 2012 by Elsevier. Reprinted with permission.
Figure 5 A drawing boundary extension (BE) task. The left panel shows two example scene stimuli that were studied for 15 s and immediately drawn from memory. The example control participants (middle and right panels) drew a more extended expanse of background than was present in the original stimuli (demonstrating BE). By contrast, the example patient’s drawings (left panel) are more accurate, showing a paradoxically better memory for the studied scenes. Reprinted from “Attenuated Boundary Extension Produces a Paradoxical Memory Advantage in Amnesic Patients,” by S. L. Mullally, H. Intraub, and E. A. Maguire, 2012, Current Biology, 22, p. 264. Copyright 2012 by Elsevier. Reprinted with permission.CC BY · PubMed Central
Figure 6 An functional magnetic resonance imaging study of boundary extension (BE; Chadwick et al., in press). (a) A modified version of the task described in Figure 4 was used with healthy participants. The analysis focused exclusively on the presentation of the first scene and contrasted trials in which the BE error was later committed with those where it was not committed. (b) This revealed activity in the hippocampus (HC) and parahippocampal cortex (PHC). Connectivity analyses showed that the HC seemed to drive the BE effect, exerting top-down influence on PHC, retrosplenial cortex (RSC), and as far back down the processing stream as early visual cortex (VC).
Figure 6 An functional magnetic resonance imaging study of boundary extension (BE; Chadwick et al., in press). (a) A modified version of the task described in Figure 4 was used with healthy participants. The analysis focused exclusively on the presentation of the first scene and contrasted trials in which the BE error was later committed with those where it was not committed. (b) This revealed activity in the hippocampus (HC) and parahippocampal cortex (PHC). Connectivity analyses showed that the HC seemed to drive the BE effect, exerting top-down influence on PHC, retrosplenial cortex (RSC), and as far back down the processing stream as early visual cortex (VC).CC BY · PubMed Central

Verification

Claims the paper makes

43 Not checked yet · 31 Own interpretation · 1 No basis given

Verify all 61 references — free account
  • It may state two separate claims as one. 17
  • Probably not a substantial claim. 6
22 of 22
  • The paper relies on this without support.

    There is currently no unified and mechanistic account of how the hippocampus supports episodic memory, imagining the future, and spatial navigation.

    “We currently lack a unified and mechanistic account of how the hippocampus supports a range of disparate cognitive functions that includes episodic memory, imagining the future, and spatial navigation.”
  • The paper relies on this without support.

    Scenes have not featured prominently in accounts of hippocampal function.

    “Up until now, scenes have not featured prominently in accounts of hippocampal function.”
  • The paper relies on this without support.

    The memory literature is awash with experiments investigating hippocampal processes that have used scene stimuli but that pay little or no attention to the effect of the scenes themselves.

    “The memory literature is awash with experiments investigating hippocampal processes (such as associative memory) that have used scene stimuli but that pay little or no attention to the effect of the scenes themselves.”
3 of 3

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Metadata

Authors
Maguire, E. A., & Mullally, S. L.
Affiliations
Wellcome Centre for Human Neuroimaging (GB)
Corresponding author
Maguire, Eleanor A.
Venue
Journal of Experimental Psychology: General
Published
2013-11
Volume
142
Issue
4
Pages
1180-1189
ISSN
  • 0096-3445 (ISSN-L)
  • 1939-2222
OpenAlex
W2103374823
Cited by
393
References
75
Citations by year
2026: 25 · 2025: 29 · 2024: 37 · 2023: 23 · 2022: 28 · 2021: 25 · 2020: 57 · 2019: 37 · 2018: 28 · 2017: 36 · 2016: 17 · 2015: 26 · 2014: 18 · 2013: 7
FWCI
12.43
Type
journal article
Language
en
Open access
Locations
  • Journal of Experimental Psychology General (publishedVersion, other-oa)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • Newcastle University ePrints (Newcastle Univesity) (cc-by)
Funders
Wellcome Trust
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Spatial Cognition and Navigation
Keywords
hippocampus, episodic memory, scene memory, spatial navigation, future imaginings, memory architecture, hippocampal dysfunction, scene construction
MeSH terms
Cognition, Hippocampus, Humans, Imagination, Memory, Space Perception, Spatial Behavior

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