1. Neuroscience

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
https://doi.org/10.7554/eLife.57313
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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, 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.

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).

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.

Metrics

  • 5,304
    views
  • 683
    downloads
  • 54
    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. 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

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Rhythmic circuit function is more robust to changes in synaptic than intrinsic conductances

    Zachary Fournier, Leandro M Alonso, Eve Marder
    Research Article

    Circuit function results from both intrinsic conductances of network neurons and the synaptic conductances that connect them. In models of neural circuits, different combinations of maximal conductances can give rise to similar activity. We compared the robustness of a neural circuit to changes in their intrinsic versus synaptic conductances. To address this, we performed a sensitivity analysis on a population of conductance-based models of the pyloric network from the crustacean stomatogastric ganglion (STG). The model network consists of three neurons with nine currents: a sodium current (Na), three potassium currents (Kd, KCa, KA), two calcium currents (CaS and CaT), a hyperpolarization-activated current (H), a non-voltage-gated leak current (leak), and a neuromodulatory current (MI). The model cells are connected by seven synapses of two types, glutamatergic and cholinergic. We produced one hundred models of the pyloric network that displayed similar activities with values of maximal conductances distributed over wide ranges. We evaluated the robustness of each model to changes in their maximal conductances. We found that individual models have different sensitivities to changes in their maximal conductances, both in their intrinsic and synaptic conductances. As expected, the models become less robust as the extent of the changes increases. Despite quantitative differences in their robustness, we found that in all cases, the model networks are more sensitive to the perturbation of their intrinsic conductances than their synaptic conductances.

    1. Neuroscience

    Cognition: When working memory works for our goals

    Jacob A Miller
    Insight

    When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.

    1. Neuroscience

    Stimulus representation in human frontal cortex supports flexible control in working memory

    Zhujun Shao, Mengya Zhang, Qing Yu
    Research Article

    When holding visual information temporarily in working memory (WM), the neural representation of the memorandum is distributed across various cortical regions, including visual and frontal cortices. However, the role of stimulus representation in visual and frontal cortices during WM has been controversial. Here, we tested the hypothesis that stimulus representation persists in the frontal cortex to facilitate flexible control demands in WM. During functional MRI, participants flexibly switched between simple WM maintenance of visual stimulus or more complex rule-based categorization of maintained stimulus on a trial-by-trial basis. Our results demonstrated enhanced stimulus representation in the frontal cortex that tracked demands for active WM control and enhanced stimulus representation in the visual cortex that tracked demands for precise WM maintenance. This differential frontal stimulus representation traded off with the newly-generated category representation with varying control demands. Simulation using multi-module recurrent neural networks replicated human neural patterns when stimulus information was preserved for network readout. Altogether, these findings help reconcile the long-standing debate in WM research, and provide empirical and computational evidence that flexible stimulus representation in the frontal cortex during WM serves as a potential neural coding scheme to accommodate the ever-changing environment.