Dynamics and maintenance of categorical responses in primary auditory cortex during task engagement

  1. Rupesh K Chillale
  2. Shihab Shamma
  3. Srdjan Ostojic
  4. Yves Boubenec  Is a corresponding author
  1. École Normale Supérieure - PSL, France
  2. University of Maryland, United States

Abstract

Grouping sets of sounds into relevant categories is an important cognitive ability that enables the association of stimuli with appropriate goal-directed behavioral responses. In perceptual tasks, the primary auditory cortex (A1) assumes a prominent role by concurrently encoding both sound sensory features and task-related variables. Here we sought to explore the role of A1 in the initiation of sound categorization, shedding light on its involvement in this cognitive process. We trained ferrets to discriminate click trains of different rates in a Go/No-Go delayed categorization task and recorded neural activity during both active behavior and passive exposure to the same sounds. Purely categorical response components were extracted and analyzed separately from sensory responses to reveal their contributions to the overall population response throughout the trials. We found that categorical activity emerged during sound presentation in the population average and was present in both active behavioral and passive states. However, upon task engagement, categorical responses to the No-Go category became suppressed in the population code, leading to an asymmetrical representation of the Go stimuli relative to the No-Go sounds and prestimulus baseline. The population code underwent an abrupt change at stimulus offset, with sustained responses after the Go sounds during the delay period. Notably, the categorical responses observed during the stimulus period exhibited a significant correlation with those extracted from the delay epoch, suggesting an early involvement of A1 in stimulus categorization.

Data availability

Data is available on Zenodo, DOI: 10.5281/zenodo.8371083.

The following data sets were generated

Article and author information

Author details

  1. Rupesh K Chillale

    Laboratoire des Systèmes Perceptifs, École Normale Supérieure - PSL, Paris, France
    Competing interests
    No competing interests declared.
  2. Shihab Shamma

    Department of Electrical and Computer Engineering, University of Maryland, College Park, United States
    Competing interests
    No competing interests declared.
  3. Srdjan Ostojic

    Laboratoire de Neurosciences Cognitives Computationnelle (INSERM U960), École Normale Supérieure - PSL, Paris, France
    Competing interests
    Srdjan Ostojic, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7473-1223
  4. Yves Boubenec

    Laboratoire des Systèmes Perceptifs, École Normale Supérieure - PSL, Paris, France
    For correspondence
    boubenec@ens.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0106-6947

Funding

Agence Nationale de la Recherche (ANR-17-EURE-0017)

  • Rupesh K Chillale
  • Shihab Shamma
  • Srdjan Ostojic
  • Yves Boubenec

Agence Nationale de la Recherche (ANR-10-IDEX-0001-02)

  • Rupesh K Chillale
  • Shihab Shamma
  • Srdjan Ostojic
  • Yves Boubenec

Agence Nationale de la Recherche (ANR-JCJC-DynaMiC)

  • Yves Boubenec

H2020 European Research Council (ERC 787836-NEUME)

  • Shihab Shamma

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Andrew J King, University of Oxford, United Kingdom

Ethics

Animal experimentation: Experiments were approved by the French Ministry of Agriculture (protocol authorization: 21022) andstrictly comply with the European directives on the protection of animals used for scientific purposes(2010/63/EU).

Version history

  1. Preprint posted: December 20, 2022 (view preprint)
  2. Received: December 20, 2022
  3. Accepted: November 12, 2023
  4. Accepted Manuscript published: November 16, 2023 (version 1)
  5. Version of Record published: January 17, 2024 (version 2)

Copyright

© 2023, Chillale 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. Rupesh K Chillale
  2. Shihab Shamma
  3. Srdjan Ostojic
  4. Yves Boubenec
(2023)
Dynamics and maintenance of categorical responses in primary auditory cortex during task engagement
eLife 12:e85706.
https://doi.org/10.7554/eLife.85706

Share this article

https://doi.org/10.7554/eLife.85706

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