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...

Full description

Bibliographic Details
Main Authors: Amber M. Kline, Destinee A. Aponte, Hiroyuki K. Kato
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