Distinct pattern separation related transfer functions in human CA3/dentate and CA1 revealed using high-resolution fMRI and variable mnemonic similarity

Lacy, Joyce W.; Yassa, Michael A.; Stark, Shauna M.; Muftuler, L. Tugan; Stark, Craig E.L.

doi:10.1101/lm.1971111

Cited by 336 publications

(437 citation statements)

References 31 publications

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“…'Input' and 'output' here refer to neural representations, and in line with other authors we approximate their similarity by that between items (Motley and Kirwan, 2012;. fMRI responses consistent with these predictions have been demonstrated in hippocampus in response to items of varied 'mnemonic similarity' (defining input similarity indirectly as the probability of successful mnemonic discrimination in a separate sample; Lacy et al, 2011), or varied viewing angle relative to previous images (Motley and Kirwan, 2012).…”

Section: Introductionsupporting

confidence: 61%

“…However, unlike previous studies our analysis was unconstrained by the direction of the repetition suppression or enhancement effect, rather than limited to regions showing repetition suppression (e.g., Bakker et al, 2008;Lacy et al, 2011). Our inclusion of regions showing repetition enhancement was exploratory, but in some cases -just as for regions showing repetition suppression -was supported by findings of the predicted parametric response functions.…”

Section: Limitations and Future Directionsmentioning

confidence: 59%

“…By examining neural responses to similar images within regions showing differential activity between novel and repeated images, it is assumed that equivalent activity between similar and novel items is consistent with pattern separation, i.e., similar images are processed as if novel, whereas equivalent activity to similar items and repetitions is consistent with pattern completion, i.e., similar items are processed as if repeated. Examining regions showing repetition suppression (Henson and Rugg, 2003), such investigations have reported activity consistent with pattern separation in a region spanning DG/CA3, and pattern completion activity in CA1 and elsewhere in the medial temporal lobe (MTL) (Bakker et al, 2008;Lacy et al, 2011). Although pattern separation and completion investigations have focussed on the role of the hippocampus, networks throughout the brain are thought to perform similar functions, including sensory cortex (Aimone et al, 2011;Gilbert and Kesner, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Cortical pattern separation and item-specific memory encoding

Pidgeon

Morcom

2016

Neuropsychologia

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Pattern separation and pattern completion are fundamental brain processes thought to be critical for episodic memory encoding and retrieval, and for discrimination between similar memories. These processes are best understood in the hippocampus, but are proposed to occur throughout the brain, in particular in sensory regions. Cortical, as well as hippocampal, pattern separation may therefore support formation of event-unique memory traces. Using fMRI, we investigated cortical pattern separation and pattern completion and their relationship to encoding activity predicting subsequent item-specific compared to gist memory. During scanning, participants viewed images of novel objects, repeated objects, and objects which were both perceptually and conceptually similar to previously presented images, while performing a size judgement task. In a later surprise recognition test, they judged whether test items were 'same' 'similar' or 'new' relative to studied items. Activity consistent with pattern separation -responses to similar items as if novel -was observed in bilateral occipito-temporal cortex. Activity consistent with pattern completion -responses to similar items as if repeated -was observed in left prefrontal cortex and hippocampus. Curve fitting analysis further revealed that graded responses to change in image conceptual and perceptual similarity in bilateral prefrontal and right parietal regions met specific computational predictions for pattern separation for one or both of these similarity dimensions. Functional overlap between encoding activity predicting subsequent item-specific recognition and pattern separation activity was also observed in left occipital cortex and bilateral inferior frontal cortex. The findings suggest that extrahippocampal regions including sensory and prefrontal cortex contribute to pattern separation and pattern completion of visual input, consistent with the proposal that cortical pattern separation contributes to formation of item-specific memory traces, facilitating accurate recognition memory.

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Section: Introductionsupporting

confidence: 61%

Section: Limitations and Future Directionsmentioning

confidence: 59%

Section: Introductionmentioning

confidence: 99%

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Cortical pattern separation and item-specific memory encoding

Pidgeon

Morcom

2016

Neuropsychologia

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“…When we experience an event, pattern separation leads to the formation of a distinct neural representation within region CA3 (8)(9)(10)(11). At retrieval, a previously stored memory representation within CA3 can be reactivated through the process of pattern completion (12,13).…”

mentioning

confidence: 99%

CA3 size predicts the precision of memory recall

Chadwick

Bonnici

Maguire

2014

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

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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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“…This computational view of dentate gyrus function is known as pattern separation, which is the process of establishing independent and nonoverlapping new memories . The critical role of dentate gyrus in pattern separation has been well established with behavioral, specific subfields lesions, gene knock-out and electrophysiological experiments in rodents (Goodrich-Hunsaker, Hunsaker, & Kesner, 2008;Leutgeb, Leutgeb, Moser, & Moser, 2007;McHugh et al, 2007;Neunuebel & Knierim, 2014) but also with functional MRI in humans (Bakker, Kirwan, Miller, & Stark, 2008;Berron et al, 2016;Lacy, Yassa, Stark, Muftuler, & Stark, 2011) where representation of similar events was always less overlapping in dentate gyrus than in the other hippocampal subfields (Berron et al, 2016). The complementary process to pattern separation is pattern completion, defined as the ability to complete a whole memory when just a partial cue for retrieval is presented.…”

Section: Introductionmentioning

confidence: 99%