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Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices

Animals sense sounds through hierarchical neural pathways that ultimately reach higher-order cortices to extract complex acoustic features, such as vocalizations. Elucidating how spectrotemporal integration varies along the hierarchy from primary to higher-order auditory cortices is a crucial step i...

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Autores principales: Kline, Amber M., Aponte, Destinee A., Kato, Hiroyuki K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10175507/
https://www.ncbi.nlm.nih.gov/pubmed/37169827
http://dx.doi.org/10.1038/s41598-023-34731-6
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author Kline, Amber M.
Aponte, Destinee A.
Kato, Hiroyuki K.
author_facet Kline, Amber M.
Aponte, Destinee A.
Kato, Hiroyuki K.
author_sort Kline, Amber M.
collection PubMed
description Animals sense sounds through hierarchical neural pathways that ultimately reach higher-order cortices to extract complex acoustic features, such as vocalizations. Elucidating how spectrotemporal integration varies along the hierarchy from primary to higher-order auditory cortices is a crucial step in understanding this elaborate sensory computation. Here we used two-photon calcium imaging and two-tone stimuli with various frequency-timing combinations to compare spectrotemporal integration between primary (A1) and secondary (A2) auditory cortices in mice. Individual neurons showed mixed supralinear and sublinear integration in a frequency-timing combination-specific manner, and we found unique integration patterns in these two areas. Temporally asymmetric spectrotemporal integration in A1 neurons suggested their roles in discriminating frequency-modulated sweep directions. In contrast, temporally symmetric and coincidence-preferring integration in A2 neurons made them ideal spectral integrators of concurrent multifrequency sounds. Moreover, the ensemble neural activity in A2 was sensitive to two-tone timings, and coincident two-tones evoked distinct ensemble activity patterns from the linear sum of component tones. Together, these results demonstrate distinct roles of A1 and A2 in encoding complex acoustic features, potentially suggesting parallel rather than sequential information extraction between these regions.
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spelling pubmed-101755072023-05-13 Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices Kline, Amber M. Aponte, Destinee A. Kato, Hiroyuki K. Sci Rep Article Animals sense sounds through hierarchical neural pathways that ultimately reach higher-order cortices to extract complex acoustic features, such as vocalizations. Elucidating how spectrotemporal integration varies along the hierarchy from primary to higher-order auditory cortices is a crucial step in understanding this elaborate sensory computation. Here we used two-photon calcium imaging and two-tone stimuli with various frequency-timing combinations to compare spectrotemporal integration between primary (A1) and secondary (A2) auditory cortices in mice. Individual neurons showed mixed supralinear and sublinear integration in a frequency-timing combination-specific manner, and we found unique integration patterns in these two areas. Temporally asymmetric spectrotemporal integration in A1 neurons suggested their roles in discriminating frequency-modulated sweep directions. In contrast, temporally symmetric and coincidence-preferring integration in A2 neurons made them ideal spectral integrators of concurrent multifrequency sounds. Moreover, the ensemble neural activity in A2 was sensitive to two-tone timings, and coincident two-tones evoked distinct ensemble activity patterns from the linear sum of component tones. Together, these results demonstrate distinct roles of A1 and A2 in encoding complex acoustic features, potentially suggesting parallel rather than sequential information extraction between these regions. Nature Publishing Group UK 2023-05-11 /pmc/articles/PMC10175507/ /pubmed/37169827 http://dx.doi.org/10.1038/s41598-023-34731-6 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Kline, Amber M.
Aponte, Destinee A.
Kato, Hiroyuki K.
Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices
title Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices
title_full Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices
title_fullStr Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices
title_full_unstemmed Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices
title_short Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices
title_sort distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10175507/
https://www.ncbi.nlm.nih.gov/pubmed/37169827
http://dx.doi.org/10.1038/s41598-023-34731-6
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