Response outcome gates the effect of spontaneous cortical state fluctuations on perceptual decisions

Abstract

Sensory responses of cortical neurons are more discriminable when evoked on a baseline of desynchronized spontaneous activity, but cortical desynchronization has not generally been associated with more accurate perceptual decisions. Here we show that mice perform more accurate auditory judgements when activity in the auditory cortex is elevated and desynchronized before stimulus onset, but only if the previous trial was an error, and that this relationship is occluded if previous outcome is ignored. We confirmed that the outcome-dependent effect of brain state on performance is neither due to idiosyncratic associations between the slow components of either signal, nor to the existence of specific cortical states evident only after errors. Instead, errors appear to gate the effect of cortical state fluctuations on discrimination accuracy. Neither facial movements nor pupil size during the baseline were associated with accuracy, but they were predictive of measures of responsivity, such as the probability of not responding to the stimulus or of responding prematurely. These results suggest that the functional role of cortical state on behavior is dynamic and constantly regulated by performance monitoring systems.

Data availability

All data and code necessary to reproduce the main findings of this manuscript are deposited on Dryad (https://dx.doi.org/10.5061/dryad.w0vt4b8vf).

The following data sets were generated

Article and author information

Author details

  1. Davide Reato

    Champalimaud Research, Champalimaud Foundation, Lisbon, Portugal
    For correspondence
    davide.reato@neuro.fchampalimaud.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5362-4616
  2. Raphael Steinfeld

    Champalimaud Research, Champalimaud Foundation, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  3. André Tacão-Monteiro

    Champalimaud Research, Champalimaud Foundation, Lisbon, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  4. Alfonso Renart

    Champalimaud Research, Champalimaud Foundation, Lisbon, Portugal
    For correspondence
    alfonso.renart@neuro.fchampalimaud.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7916-9930

Funding

Fundação para a Ciência e a Tecnologia (Postdoctoral fellowship,SFRH/BPD/119737/2016)

  • Davide Reato

H2020 Marie Skłodowska-Curie Actions (Postdoctoral fellowship,H2020-MSCA-IF-2016 75381)

  • Davide Reato

Fundação para a Ciência e a Tecnologia (Doctoral fellowships)

  • Raphael Steinfeld

Fundação Champalimaud

  • Alfonso Renart

Marie Curie Career Integration Grant (PCIG11-GA-2012-322339)

  • Alfonso Renart

Human Frontier Science Program (Young Investigator Award,RGY0089)

  • Alfonso Renart

EU FP7 (ICT-2011-9-600925)

  • Alfonso Renart

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 procedures were reviewed and approved by the Champalimaud Centre for the Unknown animalwelfare committee and approved by the Portuguese Direção Geral de Veterinária (Ref. No.6090421/000/000/2019).

Copyright

© 2023, Reato 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. Davide Reato
  2. Raphael Steinfeld
  3. André Tacão-Monteiro
  4. Alfonso Renart
(2023)
Response outcome gates the effect of spontaneous cortical state fluctuations on perceptual decisions
eLife 12:e81774.
https://doi.org/10.7554/eLife.81774

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https://doi.org/10.7554/eLife.81774