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

The hippocampus: a manifesto for change

Open access
Maguire, Eleanor A., Mullally, Sinéad L.·2013·Journal of Experimental Psychology: General
DOI 10.1037/a0033650PMC PMC3906798
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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.

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.

Claims the paper makes

0 of 61 cited sources checked · 0 supported · 0 flagged

  • Premisecitation

    Seven patients with selective bilateral hippocampal damage and amnesia correctly identified study and test pictures as identical with greater frequency than controls, demonstrating more veridical memory.

    “Seven patients with selective bilateral hippocampal damage and amnesia correctly identified that the study and test pictures were identical with greater frequency than controls, demonstrating more veridical memory (see Figure 4b).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mullally, Intraub, & Maguire, 2012

      Not checked in the free run.

  • Interpretationcitation

    The hippocampus facilitates the construction of atemporal scenes allowing event details of episodic memories and imagined future experiences to be marshaled, bound and played out in a coherent spatial context.

    “The SCT posits that the hippocampus facilitates the construction of atemporal scenes allowing the event details of episodic memories and imagined future experiences to be martialed, bound and played out in a coherent spatial context.”
    Quote in the paperSubstantial claim
  • Interpretationreasoning

    The boundary extension effect requires intact scene construction because it involves active extrapolation of the scene beyond its physical boundaries resulting in an internally generated extended scene representation.

    “The first (the BE effect) requires intact scene construction because it involves the active extrapolation of the scene beyond its physical boundaries resulting in an internally generated “extended scene” representation, which persists when the scene is no longer visible.”
    Quote in the paperSubstantial claim
  • Premisecitation

    In drawing and haptic boundary extension tasks, amnesic patients' boundary extension was greatly attenuated.

    “In both instances, the amnesic patients’ BE was greatly attenuated.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mullally, Intraub, & Maguire, 2012

      Not checked in the free run.

  • Interpretationreasoning

    These cognitive functions each require a crucial ingredient supplied by the hippocampus: the ability to internally construct spatially coherent scenes.

    “SCT proposes that despite the differences between them, these functions each require a crucial ingredient that is supplied by the hippocampus, and that is the ability to internally construct spatially coherent scenes.”
    Quote in the paperSubstantial claim
  • May combine two claims. 17
  • Classified as probably not a substantial claim. 6

  • May combine two claims.

    Premisecitation

    In the haptic task, patients' reconstructed scene area did not differ significantly from the studied scenes, whereas controls' reconstructed scenes were significantly larger than the studied scenes.

    “Although the margins for error here were large, the patients’ placement of the borders was so accurate that the area of their reconstructed scenes did not differ significantly from the area of the studied scenes. This was not the case for controls, whose reconstructed scenes were significantly larger than the studied scenes.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mullally, Intraub, & Maguire, 2012

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Imagining scenes accounted best for activity in the hippocampus and medial temporal lobes, whereas other regions were concerned with the self and time.

    “Andrews-Hanna, Reidler, Sepulcre, Poulin, and Buckner (2010) showed that imagining scenes actually accounted best for activity in the hippocampus and medial temporal lobes, whereas other regions were concerned with the self and time.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Andrews-Hanna, Reidler, Sepulcre, Poulin, and Buckner, 2010

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    These patients made significantly fewer boundary-extension-driven errors, whereas random errors did not differ between groups.

    “They also made significantly fewer BE-driven errors (“closer-up” responses), whereas the number of random errors (“farther away” responses) did not differ between the groups.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Mullally, Intraub, & Maguire, 2012

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Episodic memory subsumes multiple cognitive processes, some of which are not hippocampal dependent.

    “We know this because episodic memory subsumes multiple cognitive processes, some of which are not hippocampal dependent (Nyberg, Kim, Habib, Levine, & Tulving, 2010).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Nyberg, Kim, Habib, Levine, & Tulving, 2010

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Scene construction underpins episodic memory, imagining the future, and spatial navigation, and perhaps mind wandering and dreaming.

    “In this way, scene construction is held to underpin not only episodic memory and imagining the future but also cognitive functions such as spatial navigation (see Figure 2), and perhaps even mind wandering and dreaming.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Hippocampal activity is correlated with the number of boundaries imagined during fMRI, and place cell activity becomes less spatially specific when boundaries are removed.

    “The findings that hippocampal activity appears to be correlated with the number of boundaries imagined during fMRI (Bird, Capponi, King, Doeller, & Burgess, 2010) and place cell activity becomes less spatially specific when boundaries are removed (Barry et al., 2006) appear to bolster this argument.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Bird, Capponi, King, Doeller, & Burgess, 2010

      Not checked in the free run.

    • cites Barry et al., 2006

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Cognitive map theory posits that a fundamental function of the hippocampus is the construction and maintenance of allocentric spatial maps of the environment.

    “This led to the cognitive map theory, which posits that a fundamental function of the hippocampus is the construction and maintenance of allocentric spatial maps of the environment (O’Keefe & Nadel, 1978).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites O’Keefe & Nadel, 1978

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    The primary role of the hippocampus is not mnemonic.

    “The implication of this view is that the primary role of the hippocampus is not mnemonic.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Visual imagery boosts paired-associate recall in healthy participants and enabled patients with left temporal lobectomies to partially compensate for their verbal memory deficits.

    “Despite the rise and fall of imagery-based memory theories across the decades (Paivio, 1969), there is much evidence to suggest that visual imagery not only boosts paired-associate recall in healthy participants but also enabled patients with left temporal lobectomies to partially compensate for their verbal memory deficits (Jones, 1974).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Paivio, 1969

      Not checked in the free run.

    • cites Jones, 1974

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In healthy controls, extrapolation of scenes (the boundary extension effect) occurred rapidly around the time a scene was first viewed and was associated with engagement of the hippocampus and parahippocampal cortex.

    “Chadwick, Mullally, and Maguire (in press) found that in healthy controls, the extrapolation of scenes (the BE effect) occurred rapidly around the time a scene was first viewed and was associated with engagement of the hippocampus and parahippocampal cortex (PHC; see Figure 6).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Chadwick, Mullally, and Maguire, in press

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    Within SCT, scene construction is viewed as an essential component of episodic memory, without which episodic memories could not be truly and vividly expressed.

    “Rather, scene construction is viewed as an essential component of episodic memory without which episodic memories could not be truly and vividly expressed.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    The hippocampus drives an automatic, anticipatory scene construction process, the product of which is fed back down the processing stream, enabling other areas to express the subjective experience of a seamless and continuous reality.

    “Instead, we suggest the hippocampus drives this automatic, anticipatory scene construction process, the product of which is fed back down the processing stream, enabling other areas to express the subjective experience of a seamless and continuous reality.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given

    SCT is unique, as no other theory of hippocampal function has scenes at its core.

    “As far as we are aware, this makes SCT unique, as no other theory of hippocampal function has scenes at its core.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    The hippocampus' role in scene processing differs from parahippocampal cortex, which represents the local visual scene or three-dimensional space, and retrosplenial cortex, which may represent the most stable landmarks within an environment.

    “In this way, the hippocampus’ role in scene processing differs from the contributions of other so-called scene-selective brain regions like PHC, which is believed to represent the local visual scene (Epstein, 2008, 2011) or three-dimensional space (Mullally & Maguire, 2011; Zeidman, Mullally, Schwarzkopf, & Maguire, 2012), and retrosplenial cortex, which may play a specific role in representing”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Epstein, 2008, 2011

      Not checked in the free run.

    • cites Mullally & Maguire, 2011

      Not checked in the free run.

    • cites Auger, Mullally, & Maguire, 2012

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The finding that P01 engaged residual right hippocampus during scene construction is consistent with SCT's link between hippocampus and scene construction and inconsistent with Squire et al.'s view that P01's future imagining was not hippocampal-dependent.

    “This finding accords with SCT in linking the hippocampus with scene construction but is at odds with the view of Squire et al. (2010), who argued that “for P01 future imagining was not hippocampal-dependent” (p. 19047; see also Maguire & Hassabis, 2011).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Squire et al. (2010)

      Not checked in the free run.

    • cites Maguire & Hassabis, 2011

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    Although SCT does not preclude other mechanisms within the hippocampus, it maintains that for the hippocampus, scenes are special.

    “To summarize, although SCT does not preclude the existence of other mechanisms within the hippocampus, such as those that permit the binding of mnemonic details within a specific context (Ranganath, 2010), it maintains that for the hippocampus, scenes are special.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Ranganath, 2010

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    SCT does not permit the possibility that impaired scene construction could coexist with preserved episodic memory, because within SCT, scene construction and episodic memory are not independent processes.

    “Regardless, however, SCT does not permit the possibility that impaired scene construction could coexist with preserved episodic memory (the opposite pattern to that observed in P01) because within the SCT framework, scene construction and episodic memory are not considered to be independent processes.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    Patients with hippocampal damage may be restricted to what is in front of their eyes, deprived of a level of subjective continuity, and unable to visualize what is outside their immediate view, behind them, or around the corner.

    “They may in fact be restricted to what is in front of their eyes, deprived of a level of subjective continuity, unable to visualize what is outside of their immediate view, what is behind them, or what is just around the corner.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Interpretationcitation

    SCT holds that the hippocampus is primarily concerned with constructing scenes, which underpins episodic memory by providing the spatial backdrop, but SCT explicitly recognizes that episodic memory requires additional processes beyond scene construction.

    “Although SCT argues that the hippocampus is primarily concerned with constructing scenes, and this underpins episodic memory by providing the spatial backdrop within which an episodic memory is played out, SCT explicitly recognizes that episodic memory requires additional processes on top of this scene construction process (Hassabis & Maguire, 2007, 2009).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Hassabis & Maguire, 2007, 2009

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The BVC model views boundaries as inward bounding, whereas SCT views boundaries as outward looking, the point from which the hippocampus must extrapolate to predict and imagine the upcoming spatial environment.

    “In this way, the BVC model views boundaries as inward bounding (containing the space within specific boundaries), whereas SCT views boundaries (either physical boundaries such as walls or the edges of our current view) as outward looking, the point from which the hippocampus must extrapolate in order to make predictions about, and so imagine, the upcoming spatial environment.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    The hippocampus actively and automatically predicts and constructs the scenes we need to fuel our cognition.

    “For many of us, scenes are the language of thought, and we argue that the hippocampus actively and automatically predicts and constructs the scenes we need to fuel our cognition.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationnone given

    The construction of scenes and boundary extension involve anticipating what is likely to be beyond the view.

    “The construction of scenes and BE involve anticipating what is likely to be beyond the view.”
    Quote in the paperNot a substantial claim
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

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Previous accounts suggested that prediction and mental imagery may involve overlapping brain mechanisms, and mental imagery might have evolved from predictive brain mechanisms.

    “In fact, previous accounts suggested that prediction and mental imagery may involve overlapping brain mechanisms [6, 43, 44], and mental imagery might have evolved from predictive brain mechanisms.”

    From Decoding sound and imagery content in early visual cortex (2014) · cites this paper as [43]

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Related

Authors
Maguire, E. A., & Mullally, S. L.
Affiliations
Wellcome Centre for Human Neuroimaging (GB)
Corresponding author
Maguire, Eleanor A.
ORCID
Venue
Journal of Experimental Psychology: General
Publisher
American Psychological Association (APA)
Published
2013-11
Volume
142
Issue
4
Pages
1180-1189
ISSN
  • 0096-3445 (ISSN-L)
  • 1939-2222
DOI
10.1037/a0033650
PMC
PMC3906798
OpenAlex
W2103374823
Semantic Scholar
d2c54fbe4881e323a62d8b1d9924facd4f6a889a
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
Licence
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
  • Physical Sciences › Engineering › Automotive Engineering › 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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