1. Neuroscience

State dependent coupling of hippocampal oscillations

  1. Brijesh Modi  Is a corresponding author
  2. Matteo Guardamagna
  3. Federico Stella
  4. Marilena Griguoli
  5. Enrico Cherubini
  6. Francesco P Battaglia  Is a corresponding author
  1. European Brain Research Institute, Italy
  2. Radboud University Nijmegen, Netherlands
https://doi.org/10.7554/eLife.80263
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  1. Brijesh Modi
  2. Matteo Guardamagna
  3. Federico Stella
  4. Marilena Griguoli
  5. Enrico Cherubini
  6. Francesco P Battaglia
(2023)
State dependent coupling of hippocampal oscillations
eLife 12:e80263.
https://doi.org/10.7554/eLife.80263
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Abstract

Oscillations occurring simultaneously in a given area represent a physiological unit of brain states. They allow for temporal segmentation of spikes and support distinct behaviors. To establish how multiple oscillatory components co-varies simultaneously and influence neuronal firing during sleep and wakefulness in mice, we describe a multi-variate analytical framework for constructing the state space of hippocampal oscillations. Examining the co-occurrence patterns of oscillations on the state space, across species, uncovered the presence of network constraints and distinct set of cross-frequency interactions during wakefulness as compared to sleep. We demonstrated how the state space can be used as a canvas to map the neural firing and found that distinct neurons during navigation were tuned to different sets of simultaneously occurring oscillations during sleep. This multivariate analytical framework provides a window to move beyond classical bivariate pipelines, for investigating oscillations and neuronal firing, thereby allowing to factor-in the complexity of oscillation-population interactions.

Data availability

Datasets used in this study are available at Crcns.org (HC11 dataset) and Donders Repository (https://data.donders.ru.nl/collections/di/dcn/DSC_62002873_05_861)All codes are available made at https://github.com/brijeshmodi12/network_state_space

The following previously published data sets were used

Article and author information

Author details

  1. Brijesh Modi

    European Brain Research Institute, Rome, Italy
    For correspondence
    brijeshmodi12@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0360-1755

  2. Matteo Guardamagna

    Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.

  3. Federico Stella

    Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.

  4. Marilena Griguoli

    European Brain Research Institute, Rome, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4067-8927

  5. Enrico Cherubini

    European Brain Research Institute, Rome, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1183-2772

  6. Francesco P Battaglia

    Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, Netherlands
    For correspondence
    F.Battaglia@science.ru.nl
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Union Horizon 2020 research and innovation program MGATE (765549)

  • Francesco P Battaglia

European Union Horizon 2020 research and innovation (840704)

  • Federico Stella

ERC Advanced Grant (833964)

  • Francesco P Battaglia

Telethon (GGP16083)

  • Enrico Cherubini

Del Monte Foundation

  • Enrico Cherubini

EMBO short term fellowship (8464)

  • Brijesh Modi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: In compliance with Dutch law and institutional regulations, all animal procedures concerningrecordings from freely moving or sleeping mice were approved by the Central Commissie Dierproeven(CCD) and conducted in accordance with the Experiments on Animals Act (project number 2016-014and protocol numbers 0029).All experiments from head-restrained animals were performed in accordance with the Italian AnimalWelfare legislation (D.L. 26/2014) that implemented the European Committee Council Directive(2010/63 EEC) and were approved by local veterinary authorities, the EBRI ethical committee, andthe Italian Ministry of Health (565/PR18) All efforts were made to minimize animal suffering and toreduce the number of animals used

Reviewing Editor

  1. Antonio Fernandez-Ruiz, Cornell University, United States

Version history

  1. Preprint posted: May 4, 2022 (view preprint)
  2. Received: May 13, 2022
  3. Accepted: July 17, 2023
  4. Accepted Manuscript published: July 18, 2023 (version 1)
  5. Version of Record published: August 9, 2023 (version 2)

Copyright

© 2023, Modi et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Brijesh Modi
  2. Matteo Guardamagna
  3. Federico Stella
  4. Marilena Griguoli
  5. Enrico Cherubini
  6. Francesco P Battaglia
(2023)
State dependent coupling of hippocampal oscillations
eLife 12:e80263.
https://doi.org/10.7554/eLife.80263

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