Cortical state transitions and stimulus response evolve along stiff and sloppy parameter dimensions, respectively

  1. Adrian Ponce-Alvarez  Is a corresponding author
  2. Gabriela Mochol
  3. Ainhoa Hermoso-Mendizabal
  4. Jaime de la Rocha
  5. Gustavo Deco
  1. Universitat Pompeu Fabra, Spain
  2. Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Spain

Abstract

Previous research showed that spontaneous neuronal activity presents sloppiness: the collective behavior is strongly determined by a small number of parameter combinations, defined as 'stiff' dimensions, while it is insensitive to many others ('sloppy' dimensions). Here, we analyzed neural population activity from the auditory cortex of anesthetized rats while the brain spontaneously transited through different synchronized and desynchronized states and intermittently received sensory inputs. We showed that cortical state transitions were determined by changes in stiff parameters associated with the activity of a core of neurons with low responses to stimuli and high centrality within the observed network. In contrast, stimulus-evoked responses evolved along sloppy dimensions associated with the activity of neurons with low centrality and displaying large ongoing and stimulus-evoked fluctuations without affecting the integrity of the network. Our results shed light on the interplay among stability, flexibility, and responsiveness of neuronal collective dynamics during intrinsic and induced activity.

Data availability

We made the spiking data publicly available here:https://github.com/adrianponce/Spont_stim_spiking_A1

Article and author information

Author details

  1. Adrian Ponce-Alvarez

    Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, Spain
    For correspondence
    adrian.ponce@upf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1446-7392
  2. Gabriela Mochol

    Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Ainhoa Hermoso-Mendizabal

    Biomedical Research August Pi i Sunyer (IDIBAPS), Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Jaime de la Rocha

    Biomedical Research August Pi i Sunyer (IDIBAPS), Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3314-9384
  5. Gustavo Deco

    Center for Brain and Cognition, Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.

Funding

European Commission (Flag-Era JTC PCI2018-092891)

  • Adrian Ponce-Alvarez
  • Gustavo Deco

Horizon 2020 Framework Programme (785907 HBP SGA2)

  • Gustavo Deco

Spanish Ministry of Economy and Competitiveness (PSI2016-75688-P)

  • Gustavo Deco

Catalan Research Group Support (2017 SGR 1545)

  • Gustavo Deco

Spanish Ministry of Economy and Competitiveness together with the European Regional Development Fund Grants (SAF2010-15730)

  • Jaime de la Rocha

Spanish Ministry of Economy and Competitiveness together with the European Regional Development Fund Grants (SAF2013-46717-R)

  • Jaime de la Rocha

Spanish Ministry of Economy and Competitiveness (Juan de la Cierva Fellowship IJCI-2014-21937)

  • Gabriela Mochol

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 experiments were carried out in accordance with protocols approved by the Animal Ethics Committee of the University of Barcelona (Comité d'Experimentació Animal, Universitat de Barcelona, Reference: 116/13).

Reviewing Editor

  1. Brice Bathellier, CNRS, France

Publication history

  1. Received: November 1, 2019
  2. Accepted: March 16, 2020
  3. Accepted Manuscript published: March 17, 2020 (version 1)
  4. Version of Record published: March 31, 2020 (version 2)

Copyright

© 2020, Ponce-Alvarez 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. Adrian Ponce-Alvarez
  2. Gabriela Mochol
  3. Ainhoa Hermoso-Mendizabal
  4. Jaime de la Rocha
  5. Gustavo Deco
(2020)
Cortical state transitions and stimulus response evolve along stiff and sloppy parameter dimensions, respectively
eLife 9:e53268.
https://doi.org/10.7554/eLife.53268

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