Differential Emergence and Stability of Sensory and Temporal Representations in Context-Specific Hippocampal Sequences

Taxidis, Jiannis; Pnevmatikakis, Eftychios A.; Dorian, Conor C.; Mylavarapu, Apoorva; Arora, Jagmeet; Samadian, Kian D.; Hoffberg, Emily A.; Golshani, Peyman

doi:10.1016/j.neuron.2020.08.028

Cited by 96 publications

(140 citation statements)

References 65 publications

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“…3a and 3f ). Although the number of selective cells that we observed was relatively low, these numbers were consistent with other studies examining single unit responses to odor stimuli in these regions 8,76,77 .…”

Section: Resultssupporting

confidence: 92%

“…This selective coding is not maintained by the same ensembles during running, but instead other spatially modulated cells in CA1 and PFC maintain choice coding on the track, including the spatial delay period (common central arm on the T-maze) activity. Thus, beta-driven ensembles mediate memory-guided decision making in the hippocampal-prefrontal network, but choice selective activity is then subsequently maintained by theta-driven spatially modulated activity, similar to reports in spatial working memory tasks 77 .…”

Section: Discussionsupporting

confidence: 57%

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Rhythmic coordination of hippocampal-prefrontal ensembles for odor-place associative memory and decision making

Symanski

Bladon

Kullberg

et al. 2020

Preprint

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Associative memory recall involves brain-wide networks comprising sensory and cognitive regions, with key roles for the hippocampus and prefrontal cortex (PFC). To investigate underlying network coordination mechanisms, we monitored activity in olfactory, hippocampal, and prefrontal regions in rats performing an associative memory task in which they recalled odor-place associations to obtain reward. During recall, the beta rhythm (15-30 Hz) was prominent and coherent across the three regions for correct decisions. Furthermore, single neurons and ensembles in both hippocampus and PFC encoded recalled associations.Ensemble dynamics predicted animals' upcoming decisions and were linked specifically with beta rhythm coordination. Despite this relationship, we found that beta rhythms did not directly phase-modulate all association-coding neurons. Our findings suggest that beta rhythms coordinate ensemble activity within the hippocampal-prefrontal network to support associative memory recall and decision making, and play a permissive rather than instructive role in this process.

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Section: Resultssupporting

confidence: 92%

Section: Discussionsupporting

confidence: 57%

Rhythmic coordination of hippocampal-prefrontal ensembles for odor-place associative memory and decision making

Symanski

Bladon

Kullberg

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Compressed time cells have been observed in CA1 while holding the animal fixed in space via stationary running (Kraus et al, 2013;Salz et al, 2016;Robinson et al, 2017;Mau et al, 2018) or head-fixed restraint (Terada et al, 2017, Taxidis, et al, 2020, during a working memory delay.…”

Section: Introductionmentioning

confidence: 99%

“A compressed representation of spatial distance in the rodent hippocampus’’

Sheehan

Charczynski

Fordyce

et al. 2021

Preprint

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Principal cells in the rodent hippocampus often fire in response to traversal through a specific spatial location (place cells), as well as elapsed time during an imposed temporal delay or after stimulus offset (time cells). Sequences of time cells unfold rapidly at first, with many time cells with narrow time fields. As the triggering event recedes into the past, time cells are fewer and have broader fields. This means that the representation of time in the hippocampus is compressed with greater resolution for time points near the present. Using tetrode recordings we measured individual CA1 units while rats traveled along a track that could be changed in length. Consistent with previous results, most place cells coded for distance from the starting point of the trajectory. Critically, place cells became less numerous and showed gradually widening fields with distance from the starting location. These results suggest that as the animal leaves a landmark, the hippocampal place code forms a compressed representation of distance from the starting location. The representation of time and space in the hippocampus have similar properties suggesting that they arise from similar computational mechanisms.

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“…How changes occur during stable performance of a multi‐dimensional memory task remains an open question. Previous studies have linked the long‐term stability of a neuronal activity to different spatial locations and different task behaviors (Kentros, Agnihotri, Streater, Hawkins, & Kandel, 2004; Kinsky et al, 2020; Taxidis et al, 2020). We sought to expand on these studies by examining how different demands on long‐term memory influence the evolution of hippocampal memory representations during a task where mice pass through the same spatial location under multiple different task conditions.…”

Section: Introductionmentioning

confidence: 99%

Hippocampal spatial memory representations in mice are heterogeneously stable

et al. 2020

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The population of hippocampal neurons actively coding space continually changes across days as mice repeatedly perform tasks. Many hippocampal place cells become inactive while other previously silent neurons become active, challenging the idea that stable behaviors and memory representations are supported by stable patterns of neural activity. Active cell replacement may disambiguate unique episodes that contain overlapping memory cues, and could contribute to reorganization of memory representations. How active cell replacement affects the evolution of representations of different behaviors within a single task is unknown. We trained mice to perform a delayed nonmatching to place task over multiple weeks, and performed calcium imaging in area CA1 of the dorsal hippocampus using head‐mounted miniature microscopes. Cells active on the central stem of the maze “split” their calcium activity according to the animal's upcoming turn direction (left or right), the current task phase (study or test), or both task dimensions, even while spatial cues remained unchanged. We found that, among reliably active cells, different splitter neuron populations were replaced at unequal rates, resulting in an increasing number of cells modulated by turn direction and a decreasing number of cells with combined modulation by both turn direction and task phase. Despite continual reorganization, the ensemble code stably segregated these task dimensions. These results show that hippocampal memories can heterogeneously reorganize even while behavior is unchanging.

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Differential Emergence and Stability of Sensory and Temporal Representations in Context-Specific Hippocampal Sequences

Cited by 96 publications

References 65 publications

Rhythmic coordination of hippocampal-prefrontal ensembles for odor-place associative memory and decision making

Rhythmic coordination of hippocampal-prefrontal ensembles for odor-place associative memory and decision making

“A compressed representation of spatial distance in the rodent hippocampus’’

Hippocampal spatial memory representations in mice are heterogeneously stable

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