Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices
Abstract 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 cruci...
Main Authors: | , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Nature Portfolio
2023-05-01
|
Series: | Scientific Reports |
Online Access: | https://doi.org/10.1038/s41598-023-34731-6 |
_version_ | 1797827519949307904 |
---|---|
author | Amber M. Kline Destinee A. Aponte Hiroyuki K. Kato |
author_facet | Amber M. Kline Destinee A. Aponte Hiroyuki K. Kato |
author_sort | Amber M. Kline |
collection | DOAJ |
description | Abstract 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. |
first_indexed | 2024-04-09T12:49:38Z |
format | Article |
id | doaj.art-966d4993680048da91730de6bba333ad |
institution | Directory Open Access Journal |
issn | 2045-2322 |
language | English |
last_indexed | 2024-04-09T12:49:38Z |
publishDate | 2023-05-01 |
publisher | Nature Portfolio |
record_format | Article |
series | Scientific Reports |
spelling | doaj.art-966d4993680048da91730de6bba333ad2023-05-14T11:17:56ZengNature PortfolioScientific Reports2045-23222023-05-0113111410.1038/s41598-023-34731-6Distinct nonlinear spectrotemporal integration in primary and secondary auditory corticesAmber M. Kline0Destinee A. Aponte1Hiroyuki K. Kato2Department of Psychiatry, University of North Carolina at Chapel HillDepartment of Psychiatry, University of North Carolina at Chapel HillDepartment of Psychiatry, University of North Carolina at Chapel HillAbstract 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.https://doi.org/10.1038/s41598-023-34731-6 |
spellingShingle | Amber M. Kline Destinee A. Aponte Hiroyuki K. Kato Distinct nonlinear spectrotemporal integration in primary and secondary auditory cortices Scientific Reports |
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 |
url | https://doi.org/10.1038/s41598-023-34731-6 |
work_keys_str_mv | AT ambermkline distinctnonlinearspectrotemporalintegrationinprimaryandsecondaryauditorycortices AT destineeaaponte distinctnonlinearspectrotemporalintegrationinprimaryandsecondaryauditorycortices AT hiroyukikkato distinctnonlinearspectrotemporalintegrationinprimaryandsecondaryauditorycortices |