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.

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).

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.

Metrics

  • 815
    views
  • 145
    downloads
  • 3
    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. 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

Further reading

    1. Neuroscience
    Jacob A Miller
    Insight

    When navigating environments with changing rules, human brain circuits flexibly adapt how and where we retain information to help us achieve our immediate goals.

    1. Neuroscience
    Franziska Auer, Katherine Nardone ... David Schoppik
    Research Article

    Cerebellar dysfunction leads to postural instability. Recent work in freely moving rodents has transformed investigations of cerebellar contributions to posture. However, the combined complexity of terrestrial locomotion and the rodent cerebellum motivate new approaches to perturb cerebellar function in simpler vertebrates. Here, we adapted a validated chemogenetic tool (TRPV1/capsaicin) to describe the role of Purkinje cells — the output neurons of the cerebellar cortex — as larval zebrafish swam freely in depth. We achieved both bidirectional control (activation and ablation) of Purkinje cells while performing quantitative high-throughput assessment of posture and locomotion. Activation modified postural control in the pitch (nose-up/nose-down) axis. Similarly, ablations disrupted pitch-axis posture and fin-body coordination responsible for climbs. Postural disruption was more widespread in older larvae, offering a window into emergent roles for the developing cerebellum in the control of posture. Finally, we found that activity in Purkinje cells could individually and collectively encode tilt direction, a key feature of postural control neurons. Our findings delineate an expected role for the cerebellum in postural control and vestibular sensation in larval zebrafish, establishing the validity of TRPV1/capsaicin-mediated perturbations in a simple, genetically tractable vertebrate. Moreover, by comparing the contributions of Purkinje cell ablations to posture in time, we uncover signatures of emerging cerebellar control of posture across early development. This work takes a major step towards understanding an ancestral role of the cerebellum in regulating postural maturation.