The hippocampus is required for short‐term topographical memory in humans

Hartley, Tom T.; Bird, Chris M.; Chan, Dennis; Cipolotti, Lisa; Husain, Masud; Vargha‐Khadem, Faraneh; Burgess, Neil

doi:10.1002/hipo.20240

Cited by 313 publications

(362 citation statements)

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“…Equally, the right hippocampal representation of allocentric spatial location has long been argued to be an important component of the representation of context within episodic memory (1, 3-5, 9). This representation is also consistent with studies implicating the hippocampus [often specifically on the right (10,41)] in flexible representation of environmental topography (3,46), accurate large-scale navigation (41), and memory for arrays of locations when containing large numbers of objects (10,19) or tested from a shifted viewpoint (19).…”

Section: Discussionsupporting

confidence: 85%

Lateralized human hippocampal activity predicts navigation based on sequence or place memory

Igloi

Doeller

Berthoz

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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254

184

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The hippocampus is crucial for both spatial navigation and episodic memory, suggesting that it provides a common function to both. Here we adapt a spatial paradigm, developed for rodents, for use with functional MRI in humans to show that activation of the right hippocampus predicts the use of an allocentric spatial representation, and activation of the left hippocampus predicts the use of a sequential egocentric representation. Both representations can be identified in hippocampal activity before their effect on behavior at subsequent choice-points. Our results suggest that, rather than providing a single common function, the two hippocampi provide complementary representations for navigation, concerning places on the right and temporal sequences on the left, both of which likely contribute to different aspects of episodic memory.T he hippocampus plays a crucial role in both spatial navigation and episodic memory (1-6). However, the nature of the fundamental hippocampal process or representation that might underlie both functions remains the subject of intense speculation, including suggestions that it is best characterized as associative (7), sequential (8), flexible relational (2), allocentric (1, 5, 9), or spatial contextual (4, 5). Similar speculation surrounds the nature of any lateralization of these representations (1, 5, 10), and whether the firing of hippocampal neurons in freely moving rodents reflects allocentric position, spatial context, or sequential position along a route (5, 11, 12). Here we show that the hippocampus predicts and supports navigation via sequential representations in the left hippocampus and allocentric spatial representations in the right hippocampus. These complementary lateralized representations suggest an explanation for the multiple hippocampal contributions to different aspects of spatial and episodic memory.Within spatial memory a distinction has been made between "allocentric" (world-centered) and "egocentric" (body-centered) representations, with allocentric (or place-learning) and simple egocentric (stimulus response-like) navigation shown to depend on the hippocampus and dorsal striatum, respectively, in rodents (5, 13). recently demonstrated that an additional sequential egocentric representation depends on the rodent hippocampus. The human hippocampus has likewise been associated with allocentric representations of location, allowing accurate navigation from new starting locations (15) based on the configuration of environmental cues (16, 17) or recognition of locations from a new viewpoint (18,19). Similarly, navigation via a fixed route (15, 17) or relative to a single landmark (16), consistent with simple egocentric representations, has been associated with the dorsal striatum. However, to our knowledge, the neural bases of the sequential egocentric representation have not yet been identified in humans, and could provide a link between spatial navigation and episodic memory.Here we adapt the Starmaze task developed for mice (14,20) to investigate the neural base...

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Section: Discussionsupporting

confidence: 85%

Lateralized human hippocampal activity predicts navigation based on sequence or place memory

Igloi

Doeller

Berthoz

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

254

184

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“…Here, too, we localised HC using a working memory task, thus complementing previous studies that find evidence for HC recruitment across a range of cognitive tasks. Indeed, several studies of patients with HC atrophy have reported scene‐specific deficits for both memory and perceptual tasks [Bird et al, 2008; Hartley et al, 2007; Lee et al, 2005a, 2005b; Mullally et al, 2012; but see Kim et al, 2011, 2015]. Functional neuroimaging studies have likewise found group‐level HC activation during scene discrimination [Aly et al, 2013; Lee et al, 2008], scene construction/imagining [Zeidman et al, 2015], and working memory [Lee and Rudebeck, 2010b; Park et al, 2003].…”

Section: Discussionmentioning

confidence: 99%

“…Beyond the seminal work in both rats and non‐human primates—which identified HC cells attuned to allocentric location [O'Keefe and Nadel, 1978] and spatial view [Rolls, 1999]—recent models of human medial temporal lobe (MTL) function highlight the HC as an important structure for scene processing, via a proposed role in representing complex and conjunctive scene stimuli [Graham et al, 2010; Lee et al, 2012; Murray et al, 2007] and/or by contributions to viewpoint‐independent scene construction [Bird and Burgess, 2008; Maguire and Mullally, 2013; Zeidman et al, 2015]. These complex HC scene representations have been shown to support behavioural performance across a range of cognitive domains, including recognition memory [Bird et al, 2008; Taylor et al, 2007], short‐term memory [Hannula et al, 2006; Hartley et al, 2007], working memory [Lee and Rudebeck, 2010a, 2010b; Park et al, 2003], perceptual learning [Mundy et al, 2013], higher‐order perception [Aly et al, 2013; Barense et al, 2005, 2010; Kolarik et al, 2016; Lee et al, 2005b] and scene imagination [Hassabis et al, 2007]. …”

Section: Introductionmentioning

confidence: 99%

Evidencing a place for the hippocampus within the core scene processing network

Hodgetts

Shine

Lawrence

et al. 2016

Human Brain Mapping

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Functional neuroimaging studies have identified several “core” brain regions that are preferentially activated by scene stimuli, namely posterior parahippocampal gyrus (PHG), retrosplenial cortex (RSC), and transverse occipital sulcus (TOS). The hippocampus (HC), too, is thought to play a key role in scene processing, although no study has yet investigated scene‐sensitivity in the HC relative to these other “core” regions. Here, we characterised the frequency and consistency of individual scene‐preferential responses within these regions by analysing a large dataset (n = 51) in which participants performed a one‐back working memory task for scenes, objects, and scrambled objects. An unbiased approach was adopted by applying independently‐defined anatomical ROIs to individual‐level functional data across different voxel‐wise thresholds and spatial filters. It was found that the majority of subjects had preferential scene clusters in PHG (max = 100% of participants), RSC (max = 76%), and TOS (max = 94%). A comparable number of individuals also possessed significant scene‐related clusters within their individually defined HC ROIs (max = 88%), evidencing a HC contribution to scene processing. While probabilistic overlap maps of individual clusters showed that overlap “peaks” were close to those identified in group‐level analyses (particularly for TOS and HC), inter‐individual consistency varied across regions and statistical thresholds. The inter‐regional and inter‐individual variability revealed by these analyses has implications for how scene‐sensitive cortex is localised and interrogated in functional neuroimaging studies, particularly in medial temporal lobe regions, such as the HC. Hum Brain Mapp 37:3779–3794, 2016. © 2016 Wiley Periodicals, Inc.

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“…There has also been interest in the idea that the MTL, and the hippocampus in particular, might have a special role in spatial processing beyond its established role in memory (4,5). Several studies have reported that patients with damage to the MTL were impaired in various kinds of spatial tasks, even when the burden on memory appeared quite small and when tasks of nonspatial memory appeared less affected (6)(7)(8)(9).…”

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confidence: 99%

Medial temporal lobe and topographical memory

Urgolites

Hopkins

Squire

2017

Proc. Natl. Acad. Sci. U.S.A.

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There has been interest in the idea that medial temporal lobe (MTL) structures might be especially important for spatial processing and spatial memory. We tested the proposal that the MTL has a specific role in topographical memory as assessed in tasks of scene memory where the viewpoint shifts from study to test. Building on materials used previously for such studies, we administered three different tasks in a total of nine conditions. Participants studied a scene depicting four hills of different shapes and sizes and made a choice among four test images. In the Rotation task, the correct choice depicted the study scene from a shifted perspective. MTL patients succeeded when the study and test images were presented together but failed the moment the study scene was removed (even at a 0-s delay). In the No-Rotation task, the correct choice was a duplicate of the study scene. Patients were impaired to the same extent in the No-Rotation and Rotation tasks after matching for difficulty. Thus, an inability to accommodate changes in viewpoint does not account for patient impairment. In the Nonspatial-Perceptual task, the correct choice depicted the same overall coloring as the study scene. Patients were intact at a 2-s delay but failed at longer, distraction-filled delays. The different results for the spatial and nonspatial tasks are discussed in terms of differences in demand on working memory. We suggest that the difficulty of the spatial tasks rests on the neocortex and on the limitations of working memory, not on the MTL.hippocampus | spatial memory | working memory | long-term memory T he capacity to form declarative memory depends on the integrity of the hippocampus and related medial temporal lobe (MTL) structures (1, 2). Declarative memory provides for the representation of relationships and permits comparison among items and contexts (3). There has also been interest in the idea that the MTL, and the hippocampus in particular, might have a special role in spatial processing beyond its established role in memory (4, 5). Several studies have reported that patients with damage to the MTL were impaired in various kinds of spatial tasks, even when the burden on memory appeared quite small and when tasks of nonspatial memory appeared less affected (6-9).In one series of studies, MTL patients were impaired when they needed to appreciate a rotation in viewpoint from one perspective to another (6, 10, 11). For example, participants studied a scene depicting four hills of different shapes and sizes placed at different locations in the scene. They then decided which of four test images depicted the same study scene but now rotated from 15 to 90 degrees (6). MTL patients performed worse than controls even when a brief delay (2 s) intervened between study and test.A question arises as to whether the impairment reflects a specific difficulty in appreciating the rotation of perspective, or whether an equally severe impairment would be found even if no rotation occurred. A second question is whether the impairment reflects...

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The hippocampus is required for short‐term topographical memory in humans

Cited by 313 publications

References 100 publications

Lateralized human hippocampal activity predicts navigation based on sequence or place memory

Lateralized human hippocampal activity predicts navigation based on sequence or place memory

Evidencing a place for the hippocampus within the core scene processing network

Medial temporal lobe and topographical memory

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