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Inhibition allocates spikes during hippocampal ripples

Author

Listed:
  • Asako Noguchi

    (The University of Tokyo)

  • Roman Huszár

    (New York University)

  • Shota Morikawa

    (The University of Tokyo
    The University of Tokyo)

  • György Buzsáki

    (New York University
    NYU Langone Medical Center and Center for Neural Science)

  • Yuji Ikegaya

    (The University of Tokyo
    The University of Tokyo
    National Institute of Information and Communications Technology)

Abstract

Sets of spikes emitted sequentially across neurons constitute fundamental pulse packets in neural information processing, including offline memory replay during hippocampal sharp-wave ripples (SWRs). The relative timing of neuronal spikes is fine-tuned in each spike sequence but can vary between different sequences. However, the microcircuitry mechanism that enables such flexible spike sequencing remains unexplored. We recorded the membrane potentials of multiple hippocampal CA1 pyramidal cells in mice and found that the neurons were transiently hyperpolarized prior to SWRs. The pre-SWR hyperpolarizations were spatiotemporally heterogeneous, and larger hyperpolarizations were associated with later spikes during SWRs. Intracellular blockade of Cl−-mediated inhibition reduced pre-SWR hyperpolarizations and advanced spike times. Single-unit recordings also revealed that the pre-SWR firing rates of inhibitory interneurons predicted the SWR-relevant spike times of pyramidal cells. Thus, pre-SWR inhibitory activity determines the sequential spike times of pyramidal cells and diversifies the repertoire of sequence patterns.

Suggested Citation

  • Asako Noguchi & Roman Huszár & Shota Morikawa & György Buzsáki & Yuji Ikegaya, 2022. "Inhibition allocates spikes during hippocampal ripples," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28890-9
    DOI: 10.1038/s41467-022-28890-9
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    References listed on IDEAS

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    1. Kenneth D. Harris & Jozsef Csicsvari & Hajime Hirase & George Dragoi & György Buzsáki, 2003. "Organization of cell assemblies in the hippocampus," Nature, Nature, vol. 424(6948), pages 552-556, July.
    2. Azahara Oliva & Antonio Fernández-Ruiz & Felix Leroy & Steven A. Siegelbaum, 2020. "Hippocampal CA2 sharp-wave ripples reactivate and promote social memory," Nature, Nature, vol. 587(7833), pages 264-269, November.
    3. David J. Foster & Matthew A. Wilson, 2006. "Reverse replay of behavioural sequences in hippocampal place cells during the awake state," Nature, Nature, vol. 440(7084), pages 680-683, March.
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    Cited by:

    1. Irina Pochinok & Tristan M. Stöber & Jochen Triesch & Mattia Chini & Ileana L. Hanganu-Opatz, 2024. "A developmental increase of inhibition promotes the emergence of hippocampal ripples," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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