Mnemonic convergence in the human hippocampus

Backus, A.R.; Bosch, Sander; Ekman, Matthias; Grabovetsky, Alejandro Vicente; Doeller, Christian F.

doi:10.1038/ncomms11991

Cited by 62 publications

(61 citation statements)

References 69 publications

(89 reference statements)

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“…The role of the caudate in briefly representing locations in self-based coordinates is consistent with its role in procedural learning and stimulus-response learning (Foerde and Shohamy, 2011; Helie et al, 2013), which both require rapid pairing of environmental stimuli with action. Our results are also consistent with the view that the hippocampus is a “convergence zone” that binds relational information between event- or landmark-unique features (Davachi and DuBrow, 2015; Backus et al, 2016; Horner and Burgess, 2013; Eichenbaum, 2004). According to this view, the hippocampus plays a general role in declarative memory, which is fundamentally a relational processing system (Eichenbaum and Cohen, 2014).…”

Section: Discussionsupporting

confidence: 90%

Egocentric and allocentric visuospatial working memory in premotor Huntington's disease: A double dissociation with caudate and hippocampal volumes

et al. 2017

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Our brains represent spatial information in egocentric (self-based) or allocentric (landmark-based) coordinates. Rodent studies have demonstrated a critical role for the caudate in egocentric navigation and the hippocampus in allocentric navigation. We administered tests of egocentric and allocentric working memory to individuals with premotor Huntington’s disease (pmHD), which is associated with early caudate nucleus atrophy, and controls. Each test had 80 trials during which subjects were asked to remember 2 locations over 1-sec delays. The only difference between these otherwise identical tests was that locations could only be coded in self-based or landmark-based coordinates. We applied a multiatlas-based segmentation algorithm and computed point-wise Jacobian determinants to measure regional variations in caudate and hippocampal volumes from 3 T MRI. As predicted, the pmHD patients were significantly more impaired on egocentric working memory. Only egocentric accuracy correlated with caudate volumes, specifically the dorsolateral caudate head, right more than left, a region that receives dense efferents from dorsolateral prefrontal cortex. In contrast, only allocentric accuracy correlated with hippocampal volumes, specifically intermediate and posterior regions that connect strongly with parahippocampal and posterior parietal cortices. These results indicate that the distinction between egocentric and allocentric navigation applies to working memory. The dorsolateral caudate is important for egocentric working memory, which can explain the disproportionate impairment in pmHD. Allocentric working memory, in contrast, relies on the hippocampus and is relatively spared in pmHD.

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Section: Discussionsupporting

confidence: 90%

Egocentric and allocentric visuospatial working memory in premotor Huntington's disease: A double dissociation with caudate and hippocampal volumes

et al. 2017

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“…This contrasts with the PPA, where significant two-way image decoding was observed, in line with a role for this region in scene processing (26,27). The lack of successful two-way decoding in the HPC highlights that it is the combination of image and temporal information that is critical for HPC involvement and is consistent with a role for the HPC in associative memory (34,35) and the representation of conjunctive information (36,37). Related to this, while human studies have typically failed to observe a role for the HPC in the judgment of single durations in the order of seconds (13-16) (see also ref.…”

Section: Discussionmentioning

confidence: 80%

Evidence for the incorporation of temporal duration information in human hippocampal long-term memory sequence representations

Thavabalasingam

O’Neil

Tay

et al. 2019

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

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There has been much interest in how the hippocampus codes time in support of episodic memory. Notably, while rodent hippocampal neurons, including populations in subfield CA1, have been shown to represent the passage of time in the order of seconds between events, there is limited support for a similar mechanism in humans. Specifically, there is no clear evidence that human hippocampal activity during long-term memory processing is sensitive to temporal duration information that spans seconds. To address this gap, we asked participants to first learn short event sequences that varied in image content and interval durations. During fMRI, participants then completed a recognition memory task, as well as a recall phase in which they were required to mentally replay each sequence in as much detail as possible. We found that individual sequences could be classified using activity patterns in the anterior hippocampus during recognition memory. Critically, successful classification was dependent on the conjunction of event content and temporal structure information (with unsuccessful classification of image content or interval duration alone), and further analyses suggested that the most informative voxels resided in the anterior CA1. Additionally, a classifier trained on anterior CA1 recognition data could successfully identify individual sequences from the mental replay data, suggesting that similar activity patterns supported participants' recognition and recall memory. Our findings complement recent rodent hippocampal research, and provide evidence that long-term sequence memory representations in the human hippocampus can reflect duration information in the order of seconds. hippocampus | CA1 | episodic memory | time | functional magnetic resonance imaging S pace and time are significant dimensions of our episodic memories (1). However, while much is known about the neural substrates that contribute to spatial cognition and memory (2-4), relatively little is known about how the brain, in particular the medial temporal lobe (MTL), processes temporal information in the service of episodic memory. The discovery of rodent hippocampal time cells (5-7), which fire at specific moments during the empty delay between two events, suggests a potential hippocampal mechanism for representing the temporal structure of memories (8). Crucially, however, it is unclear whether a similar hippocampal mechanism supports human memory.Because time cells in the hippocampus (HPC) of the rodent signal the passage of time in the order of seconds, one would expect that a similar neural mechanism in humans would lead to the human HPC representing temporal duration information in the order of seconds in the context of episodic memory. To our knowledge, however, there is no existing evidence for this. No work has examined human HPC involvement in memory for temporal durations in the order of seconds within the context of long-term memory. While recent human investigations have focused on HPC contributions to the representation of temporal order,...

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“…Instead, it is the hippocampus that has been implicated in the multimodal binding that is required to form more complex event representations (Cohen et al, 1999;Damasio, 1989;Davachi, 2006;Eichenbaum et al, 2007;Horner et al, 2012). The imagery task and memoranda used here were designed to require cross-modal binding (Horner et al, 2015;Horner & Burgess, 2013 given that the hippocampus has been shown to act as a convergence zone (Backus, Bosch, Ekman, Grabovetsky, & Doeller, 2016) binding multimodal information into coherent event representations (Damasio, 1989;Marr, 1971;Teyler & DiScenna, 1986). Thus, it is possible that the differences in forgetting seen between the present studies and Brady et al (2013) relate to this dissociation between item-based perirhinal representations and event-based hippocampal representations.…”

Section: Forgetting Of Coherent Event Representationsmentioning

confidence: 99%

United we fall: All-or-none forgetting of complex episodic events

Joensen¹,

Gaskell²,

Horner³

2018

Preprint

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Do complex event representations fragment over time or are they, instead, forgotten in an all-or-none manner? For example, if we met a friend in a café and they gave us a present, do we forget the constituent elements of this event (location, person and object) independently, or would the whole event be forgotten as one? Research suggests that item-based memories are forgotten in a fragmented manner. However, we do not know how more complex episodic, ‘event-based’ memories are forgotten. We assessed both retrieval accuracy and dependency – the statistical association between the retrieval successes of different elements from the same event – for complex events. Across 4 experiments, we show that retrieval dependency is found both immediately after learning and following a 12-hour and 1-week delay. Further, the amount of retrieval dependency after a delay is greater than that predicted by a model of independent forgetting. This dependency was only seen for coherent ‘closed-loops’, where all pairwise associations between locations, people and objects were encoded. When ‘open-loops’ were learnt, where only two out of the three possible associations were encoded, no dependency was seen immediately after learning nor after a delay. Finally, we also provide evidence for higher retention rates for closed-loops than open-loops. Therefore, closed-loops do not fragment as a function of forgetting, and are retained for longer than open-loops. Our findings suggest that coherent episodic events are not only retrieved, but also forgotten, in an all-or-none manner.

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Mnemonic convergence in the human hippocampus

Cited by 62 publications

References 69 publications

Egocentric and allocentric visuospatial working memory in premotor Huntington's disease: A double dissociation with caudate and hippocampal volumes

Egocentric and allocentric visuospatial working memory in premotor Huntington's disease: A double dissociation with caudate and hippocampal volumes

Evidence for the incorporation of temporal duration information in human hippocampal long-term memory sequence representations

United we fall: All-or-none forgetting of complex episodic events

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