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

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 f...

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Main Authors: Rupesh K Chillale, Shihab Shamma, Srdjan Ostojic, Yves Boubenec
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/85706
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author Rupesh K Chillale
Shihab Shamma
Srdjan Ostojic
Yves Boubenec
author_facet Rupesh K Chillale
Shihab Shamma
Srdjan Ostojic
Yves Boubenec
author_sort Rupesh K Chillale
collection DOAJ
description 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 pre-stimulus 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.
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spelling doaj.art-59c2a16ec08e4bb08a3c8bbaef5f12342024-01-17T13:39:35ZengeLife Sciences Publications LtdeLife2050-084X2023-11-011210.7554/eLife.85706Dynamics and maintenance of categorical responses in primary auditory cortex during task engagementRupesh K Chillale0https://orcid.org/0000-0002-0858-9660Shihab Shamma1Srdjan Ostojic2https://orcid.org/0000-0002-7473-1223Yves Boubenec3https://orcid.org/0000-0002-0106-6947Laboratoire des Systèmes Perceptifs, Département d’Études Cognitives, École Normale Supérieure, PSL University,, Paris, France; Laboratoire de Neurosciences Cognitives Computationnelle (INSERM U960), Département d’Études Cognitives, École Normale Supérieure, Paris, FranceLaboratoire des Systèmes Perceptifs, Département d’Études Cognitives, École Normale Supérieure, PSL University,, Paris, France; Institute for System Research, Department of Electrical and Computer Engineering, University of Maryland, College Park, College Park, Maryland, United StatesLaboratoire de Neurosciences Cognitives Computationnelle (INSERM U960), Département d’Études Cognitives, École Normale Supérieure, Paris, FranceLaboratoire des Systèmes Perceptifs, Département d’Études Cognitives, École Normale Supérieure, PSL University,, Paris, FranceGrouping 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 pre-stimulus 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.https://elifesciences.org/articles/85706auditory cortexcategorizationpopulation codeferret
spellingShingle Rupesh K Chillale
Shihab Shamma
Srdjan Ostojic
Yves Boubenec
Dynamics and maintenance of categorical responses in primary auditory cortex during task engagement
eLife
auditory cortex
categorization
population code
ferret
title Dynamics and maintenance of categorical responses in primary auditory cortex during task engagement
title_full Dynamics and maintenance of categorical responses in primary auditory cortex during task engagement
title_fullStr Dynamics and maintenance of categorical responses in primary auditory cortex during task engagement
title_full_unstemmed Dynamics and maintenance of categorical responses in primary auditory cortex during task engagement
title_short Dynamics and maintenance of categorical responses in primary auditory cortex during task engagement
title_sort dynamics and maintenance of categorical responses in primary auditory cortex during task engagement
topic auditory cortex
categorization
population code
ferret
url https://elifesciences.org/articles/85706
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AT srdjanostojic dynamicsandmaintenanceofcategoricalresponsesinprimaryauditorycortexduringtaskengagement
AT yvesboubenec dynamicsandmaintenanceofcategoricalresponsesinprimaryauditorycortexduringtaskengagement