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Hippocampal–cortical interaction during periods of subcortical silence

Author

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  • N. K. Logothetis

    (Max Planck Institute for Biological Cybernetics, Spemannstraße 38, 72076 Tuebingen, Germany
    Centre for Imaging Sciences, Biomedical Imaging Institute, The University of Manchester, Manchester M13 9PT, UK)

  • O. Eschenko

    (Max Planck Institute for Biological Cybernetics, Spemannstraße 38, 72076 Tuebingen, Germany)

  • Y. Murayama

    (Max Planck Institute for Biological Cybernetics, Spemannstraße 38, 72076 Tuebingen, Germany)

  • M. Augath

    (Max Planck Institute for Biological Cybernetics, Spemannstraße 38, 72076 Tuebingen, Germany)

  • T. Steudel

    (Max Planck Institute for Biological Cybernetics, Spemannstraße 38, 72076 Tuebingen, Germany)

  • H. C. Evrard

    (Max Planck Institute for Biological Cybernetics, Spemannstraße 38, 72076 Tuebingen, Germany)

  • M. Besserve

    (Max Planck Institute for Biological Cybernetics, Spemannstraße 38, 72076 Tuebingen, Germany
    Max Planck Institute for Intelligent Systems, Spemannstraße 38, 72076 Tuebingen, Germany)

  • A. Oeltermann

    (Max Planck Institute for Biological Cybernetics, Spemannstraße 38, 72076 Tuebingen, Germany)

Abstract

Hippocampal ripples, episodic high-frequency field-potential oscillations primarily occurring during sleep and calmness, have been described in mice, rats, rabbits, monkeys and humans, and so far they have been associated with retention of previously acquired awake experience. Although hippocampal ripples have been studied in detail using neurophysiological methods, the global effects of ripples on the entire brain remain elusive, primarily owing to a lack of methodologies permitting concurrent hippocampal recordings and whole-brain activity mapping. By combining electrophysiological recordings in hippocampus with ripple-triggered functional magnetic resonance imaging, here we show that most of the cerebral cortex is selectively activated during the ripples, whereas most diencephalic, midbrain and brainstem regions are strongly and consistently inhibited. Analysis of regional temporal response patterns indicates that thalamic activity suppression precedes the hippocampal population burst, which itself is temporally bounded by massive activations of association and primary cortical areas. These findings suggest that during off-line memory consolidation, synergistic thalamocortical activity may be orchestrating a privileged interaction state between hippocampus and cortex by silencing the output of subcortical centres involved in sensory processing or potentially mediating procedural learning. Such a mechanism would cause minimal interference, enabling consolidation of hippocampus-dependent memory.

Suggested Citation

  • N. K. Logothetis & O. Eschenko & Y. Murayama & M. Augath & T. Steudel & H. C. Evrard & M. Besserve & A. Oeltermann, 2012. "Hippocampal–cortical interaction during periods of subcortical silence," Nature, Nature, vol. 491(7425), pages 547-553, November.
  • Handle: RePEc:nat:nature:v:491:y:2012:i:7425:d:10.1038_nature11618
    DOI: 10.1038/nature11618
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    Cited by:

    1. Rodrigo Ordoñez Sierra & Lizeth Katherine Pedraza & Lívia Barcsai & Andrea Pejin & Qun Li & Gábor Kozák & Yuichi Takeuchi & Anett J. Nagy & Magor L. Lőrincz & Orrin Devinsky & György Buzsáki & Antal B, 2023. "Closed-loop brain stimulation augments fear extinction in male rats," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Xunda Wang & Alex T. L. Leong & Shawn Z. K. Tan & Eddie C. Wong & Yilong Liu & Lee-Wei Lim & Ed X. Wu, 2023. "Functional MRI reveals brain-wide actions of thalamically-initiated oscillatory activities on associative memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    3. HaoRan Chang & Ingrid M. Esteves & Adam R. Neumann & Majid H. Mohajerani & Bruce L. McNaughton, 2023. "Cortical reactivation of spatial and non-spatial features coordinates with hippocampus to form a memory dialogue," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Haoxin Zhang & Ivan Skelin & Shiting Ma & Michelle Paff & Lilit Mnatsakanyan & Michael A. Yassa & Robert T. Knight & Jack J. Lin, 2024. "Awake ripples enhance emotional memory encoding in the human brain," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Yalin Yu & Yue Qiu & Gen Li & Kaiwei Zhang & Binshi Bo & Mengchao Pei & Jingjing Ye & Garth J. Thompson & Jing Cang & Fang Fang & Yanqiu Feng & Xiaojie Duan & Chuanjun Tong & Zhifeng Liang, 2023. "Sleep fMRI with simultaneous electrophysiology at 9.4 T in male mice," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Anli A. Liu & Simon Henin & Saman Abbaspoor & Anatol Bragin & Elizabeth A. Buffalo & Jordan S. Farrell & David J. Foster & Loren M. Frank & Tamara Gedankien & Jean Gotman & Jennifer A. Guidera & Kari , 2022. "A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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