Orchestrated ensemble activities constitute a hippocampal memory engram

Khaled Ghandour, Noriaki Ohkawa, Chi Chung Alan Fung, Hirotaka Asai, Yoshito Saitoh, Takashi Takekawa, Reiko Okubo-Suzuki, Shingo Soya, Hirofumi Nishizono, Mina Matsuo, Makoto Osanai, Masaaki Sato, Masamichi Ohkura, Junichi Nakai, Yasunori Hayashi, Takeshi Sakurai, Takashi Kitamura, Tomoki Fukai, Kaoru Inokuchi

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Article number2637
JournalNature communications
Volume10
Issue number1
DOIs
StatePublished - Dec 1 2019

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learning
Data storage equipment
Learning
cells
Neurons
neurons
Imaging systems
hippocampus
sleep
Brain
Imaging techniques
brain
retrieval
Hippocampus
Sleep
Processing
Population

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

Ghandour, K., Ohkawa, N., Fung, C. C. A., Asai, H., Saitoh, Y., Takekawa, T., ... Inokuchi, K. (2019). Orchestrated ensemble activities constitute a hippocampal memory engram. Nature communications, 10(1), [2637]. https://doi.org/10.1038/s41467-019-10683-2

Orchestrated ensemble activities constitute a hippocampal memory engram. / Ghandour, Khaled; Ohkawa, Noriaki; Fung, Chi Chung Alan; Asai, Hirotaka; Saitoh, Yoshito; Takekawa, Takashi; Okubo-Suzuki, Reiko; Soya, Shingo; Nishizono, Hirofumi; Matsuo, Mina; Osanai, Makoto; Sato, Masaaki; Ohkura, Masamichi; Nakai, Junichi; Hayashi, Yasunori; Sakurai, Takeshi; Kitamura, Takashi; Fukai, Tomoki; Inokuchi, Kaoru.

In: Nature communications, Vol. 10, No. 1, 2637, 01.12.2019.

Research output: Contribution to journalArticle

Ghandour, K, Ohkawa, N, Fung, CCA, Asai, H, Saitoh, Y, Takekawa, T, Okubo-Suzuki, R, Soya, S, Nishizono, H, Matsuo, M, Osanai, M, Sato, M, Ohkura, M, Nakai, J, Hayashi, Y, Sakurai, T, Kitamura, T, Fukai, T & Inokuchi, K 2019, 'Orchestrated ensemble activities constitute a hippocampal memory engram', Nature communications, vol. 10, no. 1, 2637. https://doi.org/10.1038/s41467-019-10683-2
Ghandour K, Ohkawa N, Fung CCA, Asai H, Saitoh Y, Takekawa T et al. Orchestrated ensemble activities constitute a hippocampal memory engram. Nature communications. 2019 Dec 1;10(1). 2637. https://doi.org/10.1038/s41467-019-10683-2
Ghandour, Khaled ; Ohkawa, Noriaki ; Fung, Chi Chung Alan ; Asai, Hirotaka ; Saitoh, Yoshito ; Takekawa, Takashi ; Okubo-Suzuki, Reiko ; Soya, Shingo ; Nishizono, Hirofumi ; Matsuo, Mina ; Osanai, Makoto ; Sato, Masaaki ; Ohkura, Masamichi ; Nakai, Junichi ; Hayashi, Yasunori ; Sakurai, Takeshi ; Kitamura, Takashi ; Fukai, Tomoki ; Inokuchi, Kaoru. / Orchestrated ensemble activities constitute a hippocampal memory engram. In: Nature communications. 2019 ; Vol. 10, No. 1.
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