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Silencing CA1 pyramidal cells output reveals the role of feedback inhibition in hippocampal oscillations

Author

Listed:
  • Chinnakkaruppan Adaikkan

    (Indian Institute of Science)

  • Justin Joseph

    (Indian Institute of Science)

  • Georgios Foustoukos

    (RIKEN Center for Brain Science
    University of Lausanne)

  • Jun Wang

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology)

  • Denis Polygalov

    (RIKEN Center for Brain Science)

  • Roman Boehringer

    (RIKEN Center for Brain Science)

  • Steven J. Middleton

    (RIKEN Center for Brain Science)

  • Arthur J. Y. Huang

    (RIKEN Center for Brain Science)

  • Li-Huei Tsai

    (Picower Institute for Learning and Memory, Massachusetts Institute of Technology
    Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Thomas J. McHugh

    (RIKEN Center for Brain Science
    The University of Tokyo)

Abstract

The precise temporal coordination of neural activity is crucial for brain function. In the hippocampus, this precision is reflected in the oscillatory rhythms observed in CA1. While it is known that a balance between excitatory and inhibitory activity is necessary to generate and maintain these oscillations, the differential contribution of feedforward and feedback inhibition remains ambiguous. Here we use conditional genetics to chronically silence CA1 pyramidal cell transmission, ablating the ability of these neurons to recruit feedback inhibition in the local circuit, while recording physiological activity in mice. We find that this intervention leads to local pathophysiological events, with ripple amplitude and intrinsic frequency becoming significantly larger and spatially triggered local population spikes locked to the trough of the theta oscillation appearing during movement. These phenotypes demonstrate that feedback inhibition is crucial in maintaining local sparsity of activation and reveal the key role of lateral inhibition in CA1 in shaping circuit function.

Suggested Citation

  • Chinnakkaruppan Adaikkan & Justin Joseph & Georgios Foustoukos & Jun Wang & Denis Polygalov & Roman Boehringer & Steven J. Middleton & Arthur J. Y. Huang & Li-Huei Tsai & Thomas J. McHugh, 2024. "Silencing CA1 pyramidal cells output reveals the role of feedback inhibition in hippocampal oscillations," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46478-3
    DOI: 10.1038/s41467-024-46478-3
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    References listed on IDEAS

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    1. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    2. Laura Lee Colgin & Tobias Denninger & Marianne Fyhn & Torkel Hafting & Tora Bonnevie & Ole Jensen & May-Britt Moser & Edvard I. Moser, 2009. "Frequency of gamma oscillations routes flow of information in the hippocampus," Nature, Nature, vol. 462(7271), pages 353-357, November.
    3. André Fisahn & Fenella G. Pike & Eberhard H. Buhl & Ole Paulsen, 1998. "Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro," Nature, Nature, vol. 394(6689), pages 186-189, July.
    4. Frederick L. Hitti & Steven A. Siegelbaum, 2014. "The hippocampal CA2 region is essential for social memory," Nature, Nature, vol. 508(7494), pages 88-92, April.
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