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

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.

Reviewing Editor

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

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

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.

Metrics

  • 922
    views
  • 186
    downloads
  • 2
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.80263

Further reading

    1. Neuroscience
    Alexandra L Jellinger, Rebecca L Suthard ... Steve Ramirez
    Research Article

    Negative memories engage a brain and body-wide stress response in humans that can alter cognition and behavior. Prolonged stress responses induce maladaptive cellular, circuit, and systems-level changes that can lead to pathological brain states and corresponding disorders in which mood and memory are affected. However, it is unclear if repeated activation of cells processing negative memories induces similar phenotypes in mice. In this study, we used an activity-dependent tagging method to access neuronal ensembles and assess their molecular characteristics. Sequencing memory engrams in mice revealed that positive (male-to-female exposure) and negative (foot shock) cells upregulated genes linked to anti- and pro-inflammatory responses, respectively. To investigate the impact of persistent activation of negative engrams, we chemogenetically activated them in the ventral hippocampus over 3 months and conducted anxiety and memory-related tests. Negative engram activation increased anxiety behaviors in both 6- and 14-month-old mice, reduced spatial working memory in older mice, impaired fear extinction in younger mice, and heightened fear generalization in both age groups. Immunohistochemistry revealed changes in microglial and astrocytic structure and number in the hippocampus. In summary, repeated activation of negative memories induces lasting cellular and behavioral abnormalities in mice, offering insights into the negative effects of chronic negative thinking-like behaviors on human health.

    1. Neuroscience
    Alexandra H Leighton, Juliette E Cheyne, Christian Lohmann
    Research Article

    Synaptic inputs to cortical neurons are highly structured in adult sensory systems, such that neighboring synapses along dendrites are activated by similar stimuli. This organization of synaptic inputs, called synaptic clustering, is required for high-fidelity signal processing, and clustered synapses can already be observed before eye opening. However, how clustered inputs emerge during development is unknown. Here, we employed concurrent in vivo whole-cell patch-clamp and dendritic calcium imaging to map spontaneous synaptic inputs to dendrites of layer 2/3 neurons in the mouse primary visual cortex during the second postnatal week until eye opening. We found that the number of functional synapses and the frequency of transmission events increase several fold during this developmental period. At the beginning of the second postnatal week, synapses assemble specifically in confined dendritic segments, whereas other segments are devoid of synapses. By the end of the second postnatal week, just before eye opening, dendrites are almost entirely covered by domains of co-active synapses. Finally, co-activity with their neighbor synapses correlates with synaptic stabilization and potentiation. Thus, clustered synapses form in distinct functional domains presumably to equip dendrites with computational modules for high-capacity sensory processing when the eyes open.