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Acquiring new memories in neocortex of hippocampal-lesioned mice

Author

Listed:
  • Wenhan Luo

    (Shanghai Tech University)

  • Di Yun

    (Shanghai Tech University)

  • Yi Hu

    (Shanghai Tech University)

  • Miaomiao Tian

    (Shanghai Tech University)

  • Jiajun Yang

    (School of Life Sciences, Tsinghua University)

  • Yifan Xu

    (School of Life Sciences, Tsinghua University)

  • Yong Tang

    (Chinese Academy of Sciences)

  • Yang Zhan

    (Chinese Academy of Sciences)

  • Hong Xie

    (Institute of Photonic Chips, University of Shanghai for Science and Technology
    University of Shanghai for Science and Technology)

  • Ji-Song Guan

    (Shanghai Tech University
    Chinese Academy of Sciences)

Abstract

The hippocampus interacts with the neocortical network for memory retrieval and consolidation. Here, we found the lateral entorhinal cortex (LEC) modulates learning-induced cortical long-range gamma synchrony (20–40 Hz) in a hippocampal-dependent manner. The long-range gamma synchrony, which was coupled to the theta (7–10 Hz) rhythm and enhanced upon learning and recall, was mediated by inter-cortical projections from layer 5 neurons of the LEC to layer 2 neurons of the sensory and association cortices. Artificially induced cortical gamma synchrony across cortical areas improved memory encoding in hippocampal lesioned mice for originally hippocampal-dependent tasks. Mechanistically, we found that activities of cortical c-Fos labeled neurons, which showed egocentric map properties, were modulated by LEC-mediated gamma synchrony during memory recall, implicating a role of cortical synchrony to generate an integrative memory representation from disperse features. Our findings reveal the hippocampal mediated organization of cortical memories and suggest brain-machine interface approaches to improve cognitive function.

Suggested Citation

  • Wenhan Luo & Di Yun & Yi Hu & Miaomiao Tian & Jiajun Yang & Yifan Xu & Yong Tang & Yang Zhan & Hong Xie & Ji-Song Guan, 2022. "Acquiring new memories in neocortex of hippocampal-lesioned mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29208-5
    DOI: 10.1038/s41467-022-29208-5
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    References listed on IDEAS

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    1. Kei M. Igarashi & Li Lu & Laura L. Colgin & May-Britt Moser & Edvard I. Moser, 2014. "Coordination of entorhinal–hippocampal ensemble activity during associative learning," Nature, Nature, vol. 510(7503), pages 143-147, June.
    2. Paul T E Cusack, 2020. "The Human Brain," Biomedical Journal of Scientific & Technical Research, Biomedical Research Network+, LLC, vol. 31(3), pages 24261-24266, October.
    3. John Lisman & Richard Morris, 2001. "Why is the cortex a slow learner?," Nature, Nature, vol. 411(6835), pages 248-249, May.
    4. Xu Liu & Steve Ramirez & Petti T. Pang & Corey B. Puryear & Arvind Govindarajan & Karl Deisseroth & Susumu Tonegawa, 2012. "Optogenetic stimulation of a hippocampal engram activates fear memory recall," Nature, Nature, vol. 484(7394), pages 381-385, April.
    5. Torkel Hafting & Marianne Fyhn & Sturla Molden & May-Britt Moser & Edvard I. Moser, 2005. "Microstructure of a spatial map in the entorhinal cortex," Nature, Nature, vol. 436(7052), pages 801-806, August.
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