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Orchestrated ensemble activities constitute a hippocampal memory engram.

ABSTRACT: The brain stores and recalls memories through a set of neurons, termed engram cells. However, it is unclear how these cells are organized to constitute a corresponding memory trace. We established a unique imaging system that combines Ca²⁺ imaging and engram identification to extract the characteristics of engram activity by visualizing and discriminating between engram and non-engram cells. Here, we show that engram cells detected in the hippocampus display higher repetitive activity than non-engram cells during novel context learning. The total activity pattern of the engram cells during learning is stable across post-learning memory processing. Within a single engram population, we detected several sub-ensembles composed of neurons collectively activated during learning. Some sub-ensembles preferentially reappear during post-learning sleep, and these replayed sub-ensembles are more likely to be reactivated during retrieval. These results indicate that sub-ensembles represent distinct pieces of information, which are then orchestrated to constitute an entire memory.

SUBMITTER: Ghandour K

PROVIDER: S-EPMC6570652 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Orchestrated ensemble activities constitute a hippocampal memory engram.

Ghandour Khaled K Ohkawa Noriaki N Fung Chi Chung Alan CCA Asai Hirotaka H Saitoh Yoshito Y Takekawa Takashi T Okubo-Suzuki Reiko R Soya Shingo S Nishizono Hirofumi H Matsuo Mina M Osanai Makoto M Sato Masaaki M Ohkura Masamichi M Nakai Junichi J Hayashi Yasunori Y Sakurai Takeshi T Kitamura Takashi T Fukai Tomoki T Inokuchi Kaoru K

Nature communications 20190614 1

The brain stores and recalls memories through a set of neurons, termed engram cells. However, it is unclear how these cells are organized to constitute a corresponding memory trace. We established a unique imaging system that combines Ca<sup>2+</sup> imaging and engram identification to extract the characteristics of engram activity by visualizing and discriminating between engram and non-engram cells. Here, we show that engram cells detected in the hippocampus display higher repetitive activity ...[more]

PMID: 31201332

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Project description:A specific memory is thought to be encoded by a sparse population of neurons. These neurons can be tagged during learning for subsequent identification and manipulation. Moreover, their ablation or inactivation results in reduced memory expression, suggesting their necessity in mnemonic processes. However, the question of sufficiency remains: it is unclear whether it is possible to elicit the behavioural output of a specific memory by directly activating a population of neurons that was active during learning. Here we show in mice that optogenetic reactivation of hippocampal neurons activated during fear conditioning is sufficient to induce freezing behaviour. We labelled a population of hippocampal dentate gyrus neurons activated during fear learning with channelrhodopsin-2 (ChR2) and later optically reactivated these neurons in a different context. The mice showed increased freezing only upon light stimulation, indicating light-induced fear memory recall. This freezing was not detected in non-fear-conditioned mice expressing ChR2 in a similar proportion of cells, nor in fear-conditioned mice with cells labelled by enhanced yellow fluorescent protein instead of ChR2. Finally, activation of cells labelled in a context not associated with fear did not evoke freezing in mice that were previously fear conditioned in a different context, suggesting that light-induced fear memory recall is context specific. Together, our findings indicate that activating a sparse but specific ensemble of hippocampal neurons that contribute to a memory engram is sufficient for the recall of that memory. Moreover, our experimental approach offers a general method of mapping cellular populations bearing memory engrams.

Dataset Information

Orchestrated ensemble activities constitute a hippocampal memory engram.

Publications

Orchestrated ensemble activities constitute a hippocampal memory engram.

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