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.

Reviewing Editor

  1. Brice Bathellier, CNRS, France

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).

Version 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.

Metrics

  • 1,541
    Page views
  • 275
    Downloads
  • 9
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. 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

Share this article

https://doi.org/10.7554/eLife.53268

Further reading

    1. Neuroscience
    Kiwamu Kudo, Kamalini G Ranasinghe ... Srikantan S Nagarajan
    Research Article

    Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.

    1. Medicine
    2. Neuroscience
    Luisa Fassi, Shachar Hochman ... Roi Cohen Kadosh
    Research Article

    In recent years, there has been debate about the effectiveness of treatments from different fields, such as neurostimulation, neurofeedback, brain training, and pharmacotherapy. This debate has been fuelled by contradictory and nuanced experimental findings. Notably, the effectiveness of a given treatment is commonly evaluated by comparing the effect of the active treatment versus the placebo on human health and/or behaviour. However, this approach neglects the individual’s subjective experience of the type of treatment she or he received in establishing treatment efficacy. Here, we show that individual differences in subjective treatment - the thought of receiving the active or placebo condition during an experiment - can explain variability in outcomes better than the actual treatment. We analysed four independent datasets (N = 387 participants), including clinical patients and healthy adults from different age groups who were exposed to different neurostimulation treatments (transcranial magnetic stimulation: Studies 1 and 2; transcranial direct current stimulation: Studies 3 and 4). Our findings show that the inclusion of subjective treatment can provide a better model fit either alone or in interaction with objective treatment (defined as the condition to which participants are assigned in the experiment). These results demonstrate the significant contribution of subjective experience in explaining the variability of clinical, cognitive, and behavioural outcomes. We advocate for existing and future studies in clinical and non-clinical research to start accounting for participants’ subjective beliefs and their interplay with objective treatment when assessing the efficacy of treatments. This approach will be crucial in providing a more accurate estimation of the treatment effect and its source, allowing the development of effective and reproducible interventions.