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Change detection in the primate auditory cortex through feedback of prediction error signals

Although cortical feedback signals are essential for modulating feedforward processing, no feedback error signal across hierarchical cortical areas has been reported. Here, we observed such a signal in the auditory cortex of awake common marmoset during an oddball paradigm to induce auditory duratio...

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Autores principales: Obara, Keitaro, Ebina, Teppei, Terada, Shin-Ichiro, Uka, Takanori, Komatsu, Misako, Takaji, Masafumi, Watakabe, Akiya, Kobayashi, Kenta, Masamizu, Yoshito, Mizukami, Hiroaki, Yamamori, Tetsuo, Kasai, Kiyoto, Matsuzaki, Masanori
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10643402/
https://www.ncbi.nlm.nih.gov/pubmed/37957168
http://dx.doi.org/10.1038/s41467-023-42553-3
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author Obara, Keitaro
Ebina, Teppei
Terada, Shin-Ichiro
Uka, Takanori
Komatsu, Misako
Takaji, Masafumi
Watakabe, Akiya
Kobayashi, Kenta
Masamizu, Yoshito
Mizukami, Hiroaki
Yamamori, Tetsuo
Kasai, Kiyoto
Matsuzaki, Masanori
author_facet Obara, Keitaro
Ebina, Teppei
Terada, Shin-Ichiro
Uka, Takanori
Komatsu, Misako
Takaji, Masafumi
Watakabe, Akiya
Kobayashi, Kenta
Masamizu, Yoshito
Mizukami, Hiroaki
Yamamori, Tetsuo
Kasai, Kiyoto
Matsuzaki, Masanori
author_sort Obara, Keitaro
collection PubMed
description Although cortical feedback signals are essential for modulating feedforward processing, no feedback error signal across hierarchical cortical areas has been reported. Here, we observed such a signal in the auditory cortex of awake common marmoset during an oddball paradigm to induce auditory duration mismatch negativity. Prediction errors to a deviant tone presentation were generated as offset calcium responses of layer 2/3 neurons in the rostral parabelt (RPB) of higher-order auditory cortex, while responses to non-deviant tones were strongly suppressed. Within several hundred milliseconds, the error signals propagated broadly into layer 1 of the primary auditory cortex (A1) and accumulated locally on top of incoming auditory signals. Blockade of RPB activity prevented deviance detection in A1. Optogenetic activation of RPB following tone presentation nonlinearly enhanced A1 tone response. Thus, the feedback error signal is critical for automatic detection of unpredicted stimuli in physiological auditory processing and may serve as backpropagation-like learning.
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spelling pubmed-106434022023-11-13 Change detection in the primate auditory cortex through feedback of prediction error signals Obara, Keitaro Ebina, Teppei Terada, Shin-Ichiro Uka, Takanori Komatsu, Misako Takaji, Masafumi Watakabe, Akiya Kobayashi, Kenta Masamizu, Yoshito Mizukami, Hiroaki Yamamori, Tetsuo Kasai, Kiyoto Matsuzaki, Masanori Nat Commun Article Although cortical feedback signals are essential for modulating feedforward processing, no feedback error signal across hierarchical cortical areas has been reported. Here, we observed such a signal in the auditory cortex of awake common marmoset during an oddball paradigm to induce auditory duration mismatch negativity. Prediction errors to a deviant tone presentation were generated as offset calcium responses of layer 2/3 neurons in the rostral parabelt (RPB) of higher-order auditory cortex, while responses to non-deviant tones were strongly suppressed. Within several hundred milliseconds, the error signals propagated broadly into layer 1 of the primary auditory cortex (A1) and accumulated locally on top of incoming auditory signals. Blockade of RPB activity prevented deviance detection in A1. Optogenetic activation of RPB following tone presentation nonlinearly enhanced A1 tone response. Thus, the feedback error signal is critical for automatic detection of unpredicted stimuli in physiological auditory processing and may serve as backpropagation-like learning. Nature Publishing Group UK 2023-11-13 /pmc/articles/PMC10643402/ /pubmed/37957168 http://dx.doi.org/10.1038/s41467-023-42553-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Obara, Keitaro
Ebina, Teppei
Terada, Shin-Ichiro
Uka, Takanori
Komatsu, Misako
Takaji, Masafumi
Watakabe, Akiya
Kobayashi, Kenta
Masamizu, Yoshito
Mizukami, Hiroaki
Yamamori, Tetsuo
Kasai, Kiyoto
Matsuzaki, Masanori
Change detection in the primate auditory cortex through feedback of prediction error signals
title Change detection in the primate auditory cortex through feedback of prediction error signals
title_full Change detection in the primate auditory cortex through feedback of prediction error signals
title_fullStr Change detection in the primate auditory cortex through feedback of prediction error signals
title_full_unstemmed Change detection in the primate auditory cortex through feedback of prediction error signals
title_short Change detection in the primate auditory cortex through feedback of prediction error signals
title_sort change detection in the primate auditory cortex through feedback of prediction error signals
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10643402/
https://www.ncbi.nlm.nih.gov/pubmed/37957168
http://dx.doi.org/10.1038/s41467-023-42553-3
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