Temporal binding function of dorsal CA1 is critical for declarative memory formation

Sellami, Azza; Abed, Alice Shaam Al; Brayda-Bruno, Laurent; Etchamendy, Nicole; Valério, Stéphane; Oulé, Marie; Pantaléon, Laura; Lamothe, Valérie; Potier, M.; Bernard, Katy; Jabourian, Maritza; Herry, Cyril; Mons, Nicole; Piazza, Pier-Vincenzo; Eichenbaum, Howard; Marighetto, Aline

doi:10.1073/pnas.1619657114

Cited by 33 publications

(59 citation statements)

References 32 publications

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“…Here we have implemented a novel experimental framework for deciphering neural coding during non-spatial, temporal associative learning in the hippocampus using chronic cellular imaging. These methods demonstrate that network dynamics during trace fear conditioning are inconsistent with hypotheses of persistent sequential [Kitamura et al, 2015, Sellami et al, 2017] or sustained [Kaminski et al, 2017] activity in CA1. Rather we find that behavioral learning in CA1 is underpinned by the emergence of a subset of cue-selective neurons with stochastic temporal dynamics across trials.…”

Section: Discussionmentioning

confidence: 83%

“…We first asked whether the hippocampus generated a consistent temporal code during each trial to connect the CS and US representations [Sellami et al, 2017, Kitamura et al, 2015]. While ordering population activity by the latency of neurons’ peak firing rates naturally lends the appearance of a sequence that spans the trial period (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In this paradigm, subjects learn that a neutral conditioned stimulus (CS) predicts an aversive, unconditioned stimulus (US), which follows the CS by a considerable time delay (the “trace” period). Circuitry within the dorsal hippocampus is required for forming these memories at trace intervals on the scale of tens of seconds [Raybuck and Lattal, 2014, Huerta et al, 2000, Quinn et al, 2005, Fendt et al, 2005, Chowdhury et al, 2005, Sellami et al, 2017]. Further, silencing activity in CA1, the output node of the hippocampus, during the trace period itself is sufficient to disrupt the temporal binding of the CS and US in memory [Sellami et al, 2017].…”

Section: Introductionmentioning

confidence: 99%

“…Previous work has proposed that persistent activity mechanisms enable the hippocampus to connect representations of events in time, bridging time gaps on the order of tens of seconds. In particular, theories suggest that representation of the neutral CS and aversive US are linked through the generation of stereotyped, sequential activity in CA1 [Kitamura et al, 2015, Sellami et al, 2017], even when animals are immobilized [MacDonald et al, 2013]. Alternatively, hippocampal activity could generate a sustained response to the CS in order to maintain a static representation of the sensory cue in working memory over the trace interval, such as in attractor models of neocortical delay period activity [Amit and Brunel, 1997, Barak and Tsodyks, 2014, Takehara-Nishiuchi and McNaughton, 2008] and recently in the human hippocampus [Kaminski et al, 2017] during working memory tasks.…”

Section: Introductionmentioning

confidence: 99%

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Hippocampal network reorganization underlies the formation of a temporal association memory

Ahmed

Priestley

Castro

et al. 2019

Preprint

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AbstractEpisodic memory requires linking events in time, a function dependent on the hippocampus. In “trace” fear conditioning, animals learn to associate a neutral cue with an aversive stimulus despite their separation in time by a delay period on the order of tens of seconds. But how this temporal association forms remains unclear. Here we use 2-photon calcium imaging to track neural population dynamics over the complete time-course of learning and show that, in contrast to previous theories, the hippocampus does not generate persistent activity to bridge the time delay. Instead, learning is concomitant with broad changes in the active neural population in CA1. While neural responses were highly stochastic in time, cue identity could be reliably read out from population activity rates over longer timescales after learning. These results question the ubiquity of neural sequences during temporal association learning, and suggest that trace fear conditioning relies on mechanisms that differ from persistent activity accounts of working memory.

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Section: Discussionmentioning

confidence: 83%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Hippocampal network reorganization underlies the formation of a temporal association memory

Ahmed

Priestley

Castro

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…Furthermore, studies that have investigated duration memory using short-term working memory tasks (13)(14)(15)(16) have often observed HPC involvement in relatively long (i.e., greater than ∼90 s) but not shorter durations, which runs counter to the proposed characteristics of time cells and the fact that studies (5)(6)(7) have observed momentto-moment time cell firing during delay periods that are less than 20 s in duration. Notably, because the HPC is suggested to be critical for sequence processing and the temporal binding of temporally discrete events (17)(18)(19)(20)(21), the involvement of this structure in representing temporal durations may be contingent on such information being embedded within a set of contiguous sequence events. Suggestive of this, we recently demonstrated using functional magnetic resonance imaging (fMRI) that human HPC activity is sensitive to changes in the durations of short intervals within event sequences (22,23).…”

mentioning

confidence: 99%

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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Intrinsic hippocampal connectivity is associated with individual differences in retrospective duration processing

et al. 2023

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The estimation of incidentally encoded durations of time intervals (retrospective duration processing) is thought to rely on the retrieval of contextual information associated with a sequence of events, automatically encoded in medial temporal lobe regions. “Time cells” have been described in the hippocampus (HC), encoding the temporal progression of events and their duration. However, whether the HC supports explicit retrospective duration judgments in humans, and which neural dynamics are involved, is still poorly understood. Here we used resting-state fMRI to test the relation between variations in intrinsic connectivity patterns of the HC, and individual differences in retrospective duration processing, assessed using a novel task involving the presentation of ecological stimuli. Results showed that retrospective duration discrimination performance predicted variations in the intrinsic connectivity of the bilateral HC with the right precentral gyrus; follow-up exploratory analyses suggested a role of the CA1 and CA4/DG subfields in driving the observed pattern. Findings provide insights on neural networks associated with implicit processing of durations in the second range.

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Temporal binding function of dorsal CA1 is critical for declarative memory formation

Cited by 33 publications

References 32 publications

Hippocampal network reorganization underlies the formation of a temporal association memory

Hippocampal network reorganization underlies the formation of a temporal association memory

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

Intrinsic hippocampal connectivity is associated with individual differences in retrospective duration processing

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