Multi-voxel pattern analysis in human hippocampal subfields

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

doi:10.3389/fnhum.2012.00290

Cited by 81 publications

(86 citation statements)

References 78 publications

(137 reference statements)

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“…The effects did not differ between art and room tasks (Ps > 0. 33). These control analyses demonstrate that the attentional state of the hippocampus-and CA2/CA3/DG in particularprovides uniquely meaningful information about memory formation.…”

Section: Predicting Memory From the Attentional State Of The Hippocampusmentioning

confidence: 75%

“…We report results for these three subfield ROIs, as well as for a single hippocampal ROI collapsing across subfield labels. Moreover, motivated by computational theories and work with animal models, which highlight different roles for CA3 and DG in memory (32), as well as recent human neuroimaging studies that have examined these regions separately (33,34), we report supplemental exploratory analyses for separate CA2/3 and DG ROIs (Fig. S1).…”

Section: Significancementioning

confidence: 99%

See 1 more Smart Citation

Attention promotes episodic encoding by stabilizing hippocampal representations

Aly

Turk‐Browne

2016

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

177

157

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Attention influences what is later remembered, but little is known about how this occurs in the brain. We hypothesized that behavioral goals modulate the attentional state of the hippocampus to prioritize goal-relevant aspects of experience for encoding. Participants viewed rooms with paintings, attending to room layouts or painting styles on different trials during high-resolution functional MRI. We identified template activity patterns in each hippocampal subfield that corresponded to the attentional state induced by each task. Participants then incidentally encoded new rooms with art while attending to the layout or painting style, and memory was subsequently tested. We found that when task-relevant information was better remembered, the hippocampus was more likely to have been in the correct attentional state during encoding. This effect was specific to the hippocampus, and not found in medial temporal lobe cortex, category-selective areas of the visual system, or elsewhere in the brain. These findings provide mechanistic insight into how attention transforms percepts into memories.long-term memory | selective attention | hippocampal subfields | medial temporal lobe | representational stability W hy do we remember some things and not others? Consider a recent experience, such as the last movie complex you visited, flight you took, or restaurant at which you ate. More information was available to your senses than was stored in memory, such as the theater number of the movie, the faces of other passengers, and the color of the napkins. The selective nature of memory is adaptive, because encoding carries a cost: newly stored memories can interfere with existing ones and with our ability to learn new information in the future. What is the mechanism by which information gets selected for encoding?Attention offers a means of prioritizing information in the environment that is most relevant to behavioral goals. Attended information, in turn, has stronger control over behavior and is represented more robustly in the brain (1, 2). If attention gates which information we perceive and act upon, then it may also determine what information we remember. Indeed, attention during encoding affects both subsequent behavioral expressions of memory (3) and the extent to which activity levels in the brain predict memory formation (4-7). Although these findings suggest that attention modulates processes related to memory, how it does so is unclear.According to biased competition and other theories of attention (1, 8), task-relevant stimuli are more robustly represented in sensory systems, and thus fare better in competition with taskirrelevant stimuli for downstream processing. Indeed, there is extensive evidence that attention enhances overall activity in visual areas that represent attended vs. unattended features and locations (2, 9). Moreover, attention modulates cortical areas of the medial temporal lobe that provide input to the hippocampus (10-12).Attention can also modulate the hippocampus itself. Specifically, there is g...

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Section: Predicting Memory From the Attentional State Of The Hippocampusmentioning

confidence: 75%

Section: Significancementioning

confidence: 99%

Attention promotes episodic encoding by stabilizing hippocampal representations

Aly

Turk‐Browne

2016

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

177

157

View full text Add to dashboard Cite

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“…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]. Studies applying multivariate analysis techniques have also found evidence that the HC contains activation patterns that are sensitive to scene‐related information [Bonnici et al, 2012; Liang et al, 2013; but see Diana et al, 2008]. Overall, these extant data, when viewed alongside the large‐scale analysis of individual‐level data reported here, suggest that the HC should be considered a key region in the putative scene processing network [see also Kornblith et al, 2013; Kreiman et al, 2000].…”

Section: Discussionmentioning

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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“…We combined high-resolution functional MRI (14) (fMRI) with an ultra-high resolution structural MRI scanning protocol that permitted the separate identification of CA1, CA3, dentate gyrus (DG), and subiculum (15,16). Stimuli were created by filming two brief action events against a green-screen background.…”

Section: Resultsmentioning

confidence: 99%

“…Manual segmentation of the hippocampal subfields was conducted using the ITK-SNAP software package (41) and a recently devised subfield segmentation protocol (15,16). It took on average 1 d to segment the subfields of one hippocampus.…”

Section: Methodsmentioning

confidence: 99%

CA3 size predicts the precision of memory recall

Chadwick

Bonnici

Maguire

2014

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

Self Cite

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There is enduring interest in why some of us have clearer memories than others, given the substantial individual variation that exists in retrieval ability and the precision with which we can differentiate past experiences. Here we report novel evidence showing that variation in the size of human hippocampal subfield CA3 predicted the amount of neural interference between episodic memories within CA3, which in turn predicted how much retrieval confusion occurred between past memories. This effect was not apparent in other hippocampal subfields. This shows that subtle individual differences in subjective mnemonic experience can be accurately gauged from measurable variations in the anatomy and neural coding of hippocampal region CA3. Moreover, this mechanism may be relevant for understanding memory muddles in aging and pathological states.O ur memories often contain overlapping elements, because they tend to feature the same people and places that form the cornerstones of our lives. Nevertheless, we are generally able to recall many of these past experiences as distinct episodes, although we are not all equally adept at doing so. There is substantial individual variation in retrieval ability and the precision with which we can differentiate past events (1, 2). This is most acute as we age and in conditions such as dementia, where confusion about the past is often evident (2). There is keen interest, therefore, in elucidating the neural mechanisms that allow us to recollect numerous life experiences despite a high degree of intermemory similarity.We know little about how this is achieved in humans, but theoretical models propose that computations within hippocampal subfields facilitate the efficient storage and retrieval of similar memories (3-7). When we experience an event, pattern separation leads to the formation of a distinct neural representation within region CA3 (8-11). At retrieval, a previously stored memory representation within CA3 can be reactivated through the process of pattern completion (12, 13). However, when episodes are highly similar, the CA3 neuronal representations may not be completely distinct, leading to partial overlap (14). It is therefore not clear precisely what the limits of CA3 pattern separation might be. Here we directly tested the capacity of human CA3 to maintain distinct episodic representations in the presence of overlapping elements. We further investigated whether variation in this ability provides an explanatory account of individual differences in the precision of episodic memory retrieval. ResultsWe combined high-resolution functional MRI (14) (fMRI) with an ultra-high resolution structural MRI scanning protocol that permitted the separate identification of CA1, CA3, dentate gyrus (DG), and subiculum (15, 16). Stimuli were created by filming two brief action events against a green-screen background. Each event was then superimposed onto the same two spatial contexts, creating four movie clips that included every combination of the two events and the two contexts (17) (Fig...

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Multi-voxel pattern analysis in human hippocampal subfields

Cited by 81 publications

References 78 publications

Attention promotes episodic encoding by stabilizing hippocampal representations

Attention promotes episodic encoding by stabilizing hippocampal representations

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

CA3 size predicts the precision of memory recall

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