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Coupling of hippocampal theta and ripples with pontogeniculooccipital waves

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  • Juan F. Ramirez-Villegas

    (Max Planck Institute for Biological Cybernetics
    Eberhard-Karls University of Tübingen
    IST Austria (Institute of Science and Technology Austria))

  • Michel Besserve

    (Max Planck Institute for Biological Cybernetics
    Max Planck Institute for Intelligent Systems)

  • Yusuke Murayama

    (Max Planck Institute for Biological Cybernetics
    International Center for Primate Brain Research)

  • Henry C. Evrard

    (Max Planck Institute for Biological Cybernetics
    International Center for Primate Brain Research
    Werner-Reichardt Centre for Integrative Neuroscience
    Orangeburg)

  • Axel Oeltermann

    (Max Planck Institute for Biological Cybernetics)

  • Nikos K. Logothetis

    (Max Planck Institute for Biological Cybernetics
    International Center for Primate Brain Research
    The University of Manchester)

Abstract

The hippocampus has a major role in encoding and consolidating long-term memories, and undergoes plastic changes during sleep1. These changes require precise homeostatic control by subcortical neuromodulatory structures2. The underlying mechanisms of this phenomenon, however, remain unknown. Here, using multi-structure recordings in macaque monkeys, we show that the brainstem transiently modulates hippocampal network events through phasic pontine waves known as pontogeniculooccipital waves (PGO waves). Two physiologically distinct types of PGO wave appear to occur sequentially, selectively influencing high-frequency ripples and low-frequency theta events, respectively. The two types of PGO wave are associated with opposite hippocampal spike-field coupling, prompting periods of high neural synchrony of neural populations during periods of ripple and theta instances. The coupling between PGO waves and ripples, classically associated with distinct sleep stages, supports the notion that a global coordination mechanism of hippocampal sleep dynamics by cholinergic pontine transients may promote systems and synaptic memory consolidation as well as synaptic homeostasis.

Suggested Citation

  • Juan F. Ramirez-Villegas & Michel Besserve & Yusuke Murayama & Henry C. Evrard & Axel Oeltermann & Nikos K. Logothetis, 2021. "Coupling of hippocampal theta and ripples with pontogeniculooccipital waves," Nature, Nature, vol. 589(7840), pages 96-102, January.
    • Handle: RePEc:nat:nature:v:589:y:2021:i:7840:d:10.1038_s41586-020-2914-4
    DOI: 10.1038/s41586-020-2914-4
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    Cited by:

    1. Amanda L. Schott & Justin Baik & Shinjae Chung & Franz Weber, 2023. "A medullary hub for controlling REM sleep and pontine waves," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Ziyue Wang & Xiang Fei & Xiaotong Liu & Yanjie Wang & Yue Hu & Wanling Peng & Ying-wei Wang & Siyu Zhang & Min Xu, 2022. "REM sleep is associated with distinct global cortical dynamics and controlled by occipital cortex," Nature Communications, Nature, vol. 13(1), pages 1-17, December.

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