Structuring Time in Human Lateral Entorhinal Cortex

Bellmund, Jacob L. S.; Deuker, Lorena; Doeller, Christian F.

doi:10.1101/458133

Cited by 8 publications

(9 citation statements)

References 70 publications

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“…Interestingly, our searchlight analysis also revealed a cluster of voxels in lateral entorhinal cortex in association with four-way sequence decoding. This cluster did not survive our a prioricorrected statistical threshold (P < 0.05 small volume correction for bilateral MTL; maximum P = 0.001 uncorrected) but is in line with recent work demonstrating the representation of temporal information in this region in rodents and humans (45)(46)(47). Although our present paradigm is unable to highlight the distinct contributions of the lateral entorhinal cortex compared with the HPC, one possibility is that distinct HPC sequence representations reflecting specific events and temporal durations may be supported by input from entorhinal cortex.…”

Section: Discussionsupporting

confidence: 86%

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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Section: Discussionsupporting

confidence: 86%

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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“…It arises spontaneously and covers the temporal granularities expected of a code supporting encoding of episodic memories. These findings are paralleled by reports from human fMRI studies reporting that activity patterns in entorhinal cortex, including its lateral part, continuously change during encoding of an experience and that the amounts of change during encoding is related to later recalled duration of the same experience (Bellmund et al, ; Lositsky et al, ). Even though it is currently not known how the temporal signals in the entorhinal–hippocampal circuits are related, it is tempting to suggest that both the formation of time cell sequences and the drifting activity in hippocampus could be driven by the temporal signals in LEC which covers both of these scales.…”

Section: Population Activity In Entorhinal Cortex and Hippocampus Varsupporting

confidence: 54%

“…The drifting representations of CA2 and CA1 arise spontaneously as required; however, the temporal drift occurs on the scales of hours that is not necessarily sufficient to capture the details of a typical episode. Recent electrophysiological studies in rodents and fMRI studies in humans suggest that a likely source of temporal information is found in the lateral entorhinal cortex (LEC) (Bellmund, Deuker, & Doeller, ; Montchal, Reagh, & Yassa, ; Tsao et al, ). We recorded LEC neurons while rats were freely foraging in an arena for 12 trials each lasting about 4 min (Figure c).…”

Section: Population Activity In Entorhinal Cortex and Hippocampus Varmentioning

confidence: 99%

Episodic memory: Neuronal codes for what, where, and when

2019

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Episodic memory is defined as the ability to recall events in a spatiotemporal context. Formation of such memories is critically dependent on the hippocampal formation and its inputs from the entorhinal cortex. To be able to support the formation of episodic memories, entorhinal cortex and hippocampal formation should contain a neuronal code that follows several requirements. First, the code should include information about position of the agent (“where”), sequence of events (“when”), and the content of the experience itself (“what”). Second, the code should arise instantly thereby being able to support memory formation of one‐shot experiences. For successful encoding and to avoid interference between memories during recall, variations in location, time, or in content of experience should result in unique ensemble activity. Finally, the code should capture several different resolutions of experience so that the necessary details relevant for future memory‐based predictions will be stored. We review how neuronal codes in entorhinal cortex and hippocampus follow these requirements and argue that during formation of episodic memories entorhinal cortex provides hippocampus with instant information about ongoing experience. Such information originates from (a) spatially modulated neurons in medial entorhinal cortex, including grid cells, which provide a stable and universal positional metric of the environment; (b) a continuously varying signal in lateral entorhinal cortex providing a code for the temporal progression of events; and (c) entorhinal neurons coding the content of experiences exemplified by object‐coding and odor‐selective neurons. During formation of episodic memories, information from these systems are thought to be encoded as unique sequential ensemble activity in hippocampus, thereby encoding associations between the content of an event and its spatial and temporal contexts. Upon exposure to parts of the encoded stimuli, activity in these ensembles can be reinstated, leading to reactivation of the encoded activity pattern and memory recollection.

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“…To match the coordinates resulting from MDS to the original positions in the virtual environment we used Procrustes analysis allowing translation, scaling, reflection and rotation (see Bellmund et al 74 for an application of the combination of multidimensional scaling and Procrustes analysis to fMRI data). The goodness of fit, the Procrustes distance, was quantified by the normalized sum of squared errors between reconstructed and true coordinates and was compared to Procrustes distances resulting from Procrustes analyses of the MDS coordinates and sets of coordinates in which the assignment of object identity to position was shuffled, yielding a surrogate distribution from all 720 possible permutations.…”

Section: Reconstructing Remembered Positionsmentioning

confidence: 99%

Deforming the metric of cognitive maps distorts memory

et al. 2019

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Environmental boundaries anchor cognitive maps that support memory. However, trapezoidal boundary geometry distorts the regular firing patterns of entorhinal grid cells proposedly providing a metric for cognitive maps. Here, we test the impact of trapezoidal boundary geometry on human spatial memory using immersive virtual reality. Consistent with reduced regularity of grid patterns in rodents and a grid-cell model based on the eigenvectors of the successor representation, human positional memory was degraded in a trapezoid compared to a square environment; an effect particularly pronounced in the trapezoid's narrow part. Congruent with spatial frequency changes of eigenvector grid patterns, distance estimates between remembered positions were persistently biased; revealing distorted memory maps that explained behavior better than the objective maps. Our findings demonstrate that environmental geometry affects human spatial memory similarly to rodent grid cell activity-thus strengthening the putative link between grid cells and behavior along with their cognitive functions beyond navigation.

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Structuring Time in Human Lateral Entorhinal Cortex

Cited by 8 publications

References 70 publications

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

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

Episodic memory: Neuronal codes for what, where, and when

Deforming the metric of cognitive maps distorts memory

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