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).

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

  • 1,623
    views
  • 284
    downloads
  • 14
    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. 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. Computational and Systems Biology
    2. Neuroscience
    Brian DePasquale, Carlos D Brody, Jonathan W Pillow
    Research Article

    Accumulating evidence to make decisions is a core cognitive function. Previous studies have tended to estimate accumulation using either neural or behavioral data alone. Here we develop a unified framework for modeling stimulus-driven behavior and multi-neuron activity simultaneously. We applied our method to choices and neural recordings from three rat brain regions - the posterior parietal cortex (PPC), the frontal orienting fields (FOF), and the anterior-dorsal striatum (ADS) - while subjects performed a pulse-based accumulation task. Each region was best described by a distinct accumulation model, which all differed from the model that best described the animal's choices. FOF activity was consistent with an accumulator where early evidence was favored while the ADS reflected near perfect accumulation. Neural responses within an accumulation framework unveiled a distinct association between each brain region and choice. Choices were better predicted from all regions using a comprehensive, accumulation-based framework and different brain regions were found to differentially reflect choice-related accumulation signals: FOF and ADS both reflected choice but ADS showed more instances of decision vacillation. Previous studies relating neural data to behaviorally-inferred accumulation dynamics have implicitly assumed that individual brain regions reflect the whole-animal level accumulator. Our results suggest that different brain regions represent accumulated evidence in dramatically different ways and that accumulation at the whole-animal level may be constructed from a variety of neural-level accumulators.

    1. Neuroscience
    Sandra P Cárdenas-García, Sundas Ijaz, Alberto E Pereda
    Research Article Updated

    Most nervous systems combine both transmitter-mediated and direct cell–cell communication, known as ‘chemical’ and ‘electrical’ synapses, respectively. Chemical synapses can be identified by their multiple structural components. Electrical synapses are, on the other hand, generally defined by the presence of a ‘gap junction’ (a cluster of intercellular channels) between two neuronal processes. However, while gap junctions provide the communicating mechanism, it is unknown whether electrical transmission requires the contribution of additional cellular structures. We investigated this question at identifiable single synaptic contacts on the zebrafish Mauthner cells, at which gap junctions coexist with specializations for neurotransmitter release and where the contact unequivocally defines the anatomical limits of a synapse. Expansion microscopy of these single contacts revealed a detailed map of the incidence and spatial distribution of proteins pertaining to various synaptic structures. Multiple gap junctions of variable size were identified by the presence of their molecular components. Remarkably, most of the synaptic contact’s surface was occupied by interleaving gap junctions and components of adherens junctions, suggesting a close functional association between these two structures. In contrast, glutamate receptors were confined to small peripheral portions of the contact, indicating that most of the synaptic area functions as an electrical synapse. Thus, our results revealed the overarching organization of an electrical synapse that operates with not one, but multiple gap junctions, in close association with structural and signaling molecules known to be components of adherens junctions. The relationship between these intercellular structures will aid in establishing the boundaries of electrical synapses found throughout animal connectomes and provide insight into the structural organization and functional diversity of electrical synapses.