Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks

  1. Víctor J López-Madrona
  2. Elena Pérez-Montoyo
  3. Efrén Álvarez-Salvado
  4. David Moratal
  5. Oscar Herreras
  6. Ernesto Pereda
  7. Claudio R Mirasso
  8. Santiago Canals  Is a corresponding author
  1. Universidad Miguel Hernández, Spain
  2. Universitat Politècnica de València, Spain
  3. Cajal Institute, Spain
  4. Universidad de La Laguna, Spain
  5. Universitat de les Illes Balears, Spain
  6. Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas and Universidad Miguel Hernández, Spain

Abstract

Hippocampal firing is organized in theta sequences controlled by internal memory processes and by external sensory cues, but how these computations are coordinated is not fully understood. Although theta activity is commonly studied as a unique coherent oscillation, it is the result of complex interactions between different rhythm generators. Here, by separating hippocampal theta activity in three different current generators, we found epochs with variable theta frequency and phase coupling, suggesting flexible interactions between theta generators. We found that epochs of highly synchronized theta rhythmicity preferentially occurred during behavioral tasks requiring coordination between internal memory representations and incoming sensory information. In addition, we found that gamma oscillations were associated with specific theta generators and the strength of theta-gamma coupling predicted the synchronization between theta generators. We propose a mechanism for segregating or integrating hippocampal computations based on the flexible coordination of different theta frameworks to accommodate the cognitive needs.

Data availability

All datasets are available at: http://dx.doi.org/10.20350/digitalCSIC/12537

The following data sets were generated

Article and author information

Author details

  1. Víctor J López-Madrona

    Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas, Universidad Miguel Hernández, San Juan de Alicante, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8234-7160
  2. Elena Pérez-Montoyo

    Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas, Universidad Miguel Hernández, San Juan de Alicante, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Efrén Álvarez-Salvado

    Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas, Universidad Miguel Hernández, San Juan de Alicante, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. David Moratal

    Centro de Biomateriales e Ingeniería Tisular, Universitat Politècnica de València, València, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Oscar Herreras

    Department of Systems Neuroscience, Cajal Institute, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8210-3710
  6. Ernesto Pereda

    Departamento de Ingeniería Industrial, Universidad de La Laguna, La Laguna, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Claudio R Mirasso

    Instituto de Física Interdisciplinar y Sistemas Complejos, Universitat de les Illes Balears, Palma de Mallorca, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2980-7038
  8. Santiago Canals

    Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas and Universidad Miguel Hernández, San Juan de Alicante, Spain
    For correspondence
    scanals@umh.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2175-8139

Funding

European Regional Development Fund (BFU2015-64380-C2-1-R)

  • Santiago Canals

European Regional Development Fund (BFU2015-64380-C2-2-R)

  • David Moratal

European Regional Development Fund (PGC2018-101055-B-I00)

  • Santiago Canals

Horizon 2020 Framework Programme (668863 (SyBil-AA))

  • Santiago Canals

Spanish State Research Agency (SEV- 2017-0723)

  • Santiago Canals

MINECO (TEC2016-80063-C3-3-R)

  • Claudio R Mirasso

MINECO (TEC2016-80063-C3-2-R)

  • Ernesto Pereda

Spanish State Research Agency (MDM-2017-0711)

  • Claudio R Mirasso

MINECO (SAF2016-80100-R)

  • Oscar Herreras

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

Reviewing Editor

  1. Martin Vinck, Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany

Ethics

Animal experimentation: All animal experiments were approved by the Animal Care and Use Committee of the Instituto de Neurociencias de Alicante, Alicante, Spain, and comply with the Spanish (law 32/2007) and European regulations (EU directive 86/609, EU decree 2001-486, and EU recommendation 2007/526/EC).

Version history

  1. Received: March 27, 2020
  2. Accepted: July 19, 2020
  3. Accepted Manuscript published: July 20, 2020 (version 1)
  4. Accepted Manuscript updated: July 22, 2020 (version 2)
  5. Version of Record published: August 7, 2020 (version 3)

Copyright

© 2020, López-Madrona 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. Víctor J López-Madrona
  2. Elena Pérez-Montoyo
  3. Efrén Álvarez-Salvado
  4. David Moratal
  5. Oscar Herreras
  6. Ernesto Pereda
  7. Claudio R Mirasso
  8. Santiago Canals
(2020)
Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks
eLife 9:e57313.
https://doi.org/10.7554/eLife.57313

Share this article

https://doi.org/10.7554/eLife.57313

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