Decoding representations of scenes in the medial temporal lobes

Bonnici, Heidi M.; Kumaran, Dharshan; Chadwick, Martin J.; Weiskopf, Nikolaus; Hassabis, Demis; Maguire, Eleanor A.

doi:10.1002/hipo.20960

Cited by 66 publications

(89 citation statements)

References 51 publications

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“…This provides a novel insight into spatial processing, and demonstrates that even during recall of internally generated, complex episodic-like memories, the hippocampus maintains a distinct representation of relevant spatial environments. It is interesting to note that we did not find any evidence for the presence of generalized spatial information within the parahippocampal cortex, a region documented to represent scene information in previous MVPA studies (e.g., Hassabis et al 2009;Bonnici et al 2011). One clear difference between this study and those previous studies is that here we examined spatial scenes that were generated as part of episodic-like memories.…”

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confidence: 60%

“…In order to do this, a classifier was trained to differentiate Memories A and B, where the event content is exactly matched, and the memories only (Lee et al 2004;Leutgeb et al 2004Leutgeb et al , 2005Leutgeb et al , 2007Vazdarjanova and Guzowski 2004;Wills et al 2005). A small number of fMRI studies in humans have produced results that are consistent with similar processes occurring in the human hippocampus (Kumaran and Maguire 2006;Bakker et al 2008;Bonnici et al 2011;Lacy et al 2011), all of which involved graded changes in pictures of objects or scenes. However, none of these studies could speak to the issue of whether pattern separation operates in the context of more complex dynamic episodic-like memories, a link that is critical to computational theories of hippocampal function.…”

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confidence: 99%

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Decoding overlapping memories in the medial temporal lobes using high-resolution fMRI

Chadwick¹,

Hassabis²,

Maguire³

2011

Learn. Mem.

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The hippocampus is proposed to process overlapping episodes as discrete memory traces, although direct evidence for this in human episodic memory is scarce. Using green-screen technology we created four highly overlapping movies of everyday events. Participants were scanned using high-resolution fMRI while recalling the movies. Multivariate pattern analysis revealed that the hippocampus supported distinct representations of each memory, while neighboring regions did not, demonstrating that the human hippocampus maintains unique pattern-separated memory traces even when memories are highly overlapping. The hippocampus also contained representations of spatial contexts that were shared across different memories, consistent with a specialized role in processing space.[Supplemental material is available for this article.]Our daily lives usually involve encounters with a relatively limited range of people and locations, and consequently, the episodic memories that are formed often contain much overlap. Nevertheless, most of the time we are able to remember each event as a distinct episode. The hippocampus has long been implicated as the critical brain structure involved in separating overlapping episodes into unique representations, which are then stored as distinct memory traces (Marr 1971;O'Reilly and McClelland 1994;Treves and Rolls 1994;McClelland and Goddard 1996;O'Reilly and Rudy 2001). While the theoretical basis for this idea has a strong grounding in the anatomy of the hippocampus and in the rodent literature (Lee et al. 2004;Leutgeb et al. 2004Leutgeb et al. , 2005Leutgeb et al. , 2007Vazdarjanova and Guzowski 2004;Wills et al. 2005), empirical evidence for the existence of traces of complex episodic memories in the human hippocampus remains scarce.A recent study demonstrated that specific episodic-like memories can be decoded solely from patterns of functional MRI (fMRI) activity across voxels in the human hippocampus using multivariate pattern analysis (MVPA) (Chadwick et al. 2010), suggesting that episodic-like memory traces are present and detectable within the human hippocampus. However, each episode in this study differed along a variety of dimensions, including the identity of the people involved, the actions performed, and the spatial contexts. It was therefore not possible to determine exactly how the event-like episodes were represented within the hippocampus, or precisely what aspect of the episodes was being detected by the MVPA classification technique.The purpose of the current study was to apply similar MVPA methods to the study of highly overlapping episodic-like memories in order to determine whether it is possible to detect unique, bound memory traces within the human hippocampus and elsewhere in the medial temporal lobes (MTL). The overlapping information in the episodes were a critical aspect of this study, as it was important to ensure that no episode could be uniquely specified by any single element within it. In order to create such fully controlled stimuli, we filmed two brief action...

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confidence: 99%

Decoding overlapping memories in the medial temporal lobes using high-resolution fMRI

Chadwick¹,

Hassabis²,

Maguire³

2011

Learn. Mem.

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“…Furthermore, future work can address what aspects of an experience modulate postencoding persistence. In the current study, distinct features of the encoding experience, including bottom-up sensory differences in the stimulus content and top-down processes (reflecting different instructions and decisions across the tasks) (35)(36)(37), could have contributed to the distinctive hippocampal patterns seen during OF and SF encoding.…”

Section: Discussionmentioning

confidence: 75%

Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory

Tambini

Davachi

2013

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

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The transformation of new experiences into lasting memories is thought to be mediated by postencoding reactivation or the reexpression of activity patterns that characterize prior encoding experiences during subsequent offline periods. Although hippocampal reactivation has been well-described in the rodent, evidence for postencoding persistence of hippocampal encoding patterns has yet to be described in humans. Using functional MRI, we examined the persistence of multivoxel hippocampal encoding patterns into postencoding rest periods. To characterize activity patterns, we computed the pairwise multivoxel correlation structure (MVCS) across hippocampal voxels during two distinct encoding tasks as well as during pre-and postencoding rest periods. We found that the hippocampal MVCS for each encoding task was more similar to the MVCS during immediate postencoding rest periods compared with a preencoding, baseline rest period. Additionally, using a principal component decomposition approach, we found that the strongest encoding patterns showed evidence of preferential persistence into immediate postencoding rest periods. Finally, the extent to which the strongest encoding patterns showed evidence of preferential persistence into immediate postencoding rest significantly correlated with later memory for stimuli seen during encoding. Taken together, these results provide strong evidence for hippocampal reactivation in humans, which was measured by the persistence of hippocampal encoding patterns into immediate postencoding rest periods, and importantly, provide a possible link between this persistence and memory consolidation.hippocampus | multivoxel pattern analysis | resting state O ur ability to remember a unique episode for days, months, and even years in the future is an impressive biological feat. Converging evidence across multiple species indicates that the hippocampus is essential for the initial formation of an episodic memory trace (1, 2). In addition to memory acquisition, the hippocampus is also thought to play a pivotal role in the postencoding stabilization of memories by restructuring how information is represented across hippocampal-neocortical networks (2-4). Specifically, hippocampal replay or the subsequent reactivation of patterns of hippocampal activity that characterize a prior experience (5-8) is hypothesized to contribute to memory consolidation (3,6,9).In line with these predictions, previous work in rodents has shown that multivariate patterns of hippocampal activity are reactivated during sleep (10-12) and awake periods (13-16). Critical for theories of consolidation, the extent of hippocampal reactivation in rodents has recently been related to spatial memory improvements (17), whereas interference with putative reactivation events leads to impairments in learning (18)(19)(20). Prior work in humans using functional MRI (fMRI) has shown that resting connectivity between the hippocampus and encoding-related cortical areas can be modulated by an associative encoding experience (21,22) and that...

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“…individual scenes and navigation-related processing. Although the cortical loci of spatial layout perception in humans have been well described (Aguirre et al, 1998;Kravitz et al, 2011b;MacEvoy and Epstein, 2011;Mullally and Maguire, 2011;Park et al, 2011;Bonnici et al, 2012), the dynamics of spatial cognition remain unexplained, partly because neuronal markers indexing spatial layout processing remain unknown, and partly because quantitative models of spatial layout processing are missing. The central questions of this study are thus twofold: First, what are the temporal dynamics with which representation of spatial layout emerge in the brain?…”

Section: Introductionmentioning

confidence: 99%

Dynamics of scene representations in the human brain revealed by magnetoencephalography and deep neural networks

Cichy

Khosla

Pantazis

et al. 2015

Preprint

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Human scene recognition is a rapid multistep process evolving over time from single scene image to spatial layout processing. We used multivariate pattern analyses on magnetoencephalography (MEG) data to unravel the time course of this cortical process. Following an early signal for lowerlevel visual analysis of single scenes at ~100 ms, we found a marker of real-world scene size, i.e. spatial layout processing, at ~250 ms indexing neural representations robust to changes in unrelated scene properties and viewing conditions. For a quantitative model of how scene size representations may arise in the brain, we compared MEG data to a deep neural network model trained on scene classification. Representations of scene size emerged intrinsically in the model, and resolved emerging neural scene size representation. Together our data provide a first description of an electrophysiological signal for layout processing in humans, and suggest that deep neural networks are a promising framework to investigate how spatial layout representations emerge in the human brain.

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Decoding representations of scenes in the medial temporal lobes

Cited by 66 publications

References 51 publications

Decoding overlapping memories in the medial temporal lobes using high-resolution fMRI

Decoding overlapping memories in the medial temporal lobes using high-resolution fMRI

Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory

Dynamics of scene representations in the human brain revealed by magnetoencephalography and deep neural networks

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