Reduced Neural Responses to Natural Foreground versus Background Sounds in the Auditory Cortex.

IF 4.4 2区 医学 Q1 NEUROSCIENCES
Gregory R Hamersky, Luke A Shaheen, Mateo López Espejo, Jereme C Wingert, Stephen V David
{"title":"Reduced Neural Responses to Natural Foreground versus Background Sounds in the Auditory Cortex.","authors":"Gregory R Hamersky, Luke A Shaheen, Mateo López Espejo, Jereme C Wingert, Stephen V David","doi":"10.1523/JNEUROSCI.0121-24.2024","DOIUrl":null,"url":null,"abstract":"<p><p>In everyday hearing, listeners face the challenge of understanding behaviorally relevant foreground stimuli (speech, vocalizations) in complex backgrounds (environmental, mechanical noise). Prior studies have shown that high-order areas of human auditory cortex (AC) preattentively form an enhanced representation of foreground stimuli in the presence of background noise. This enhancement requires identifying and grouping the features that comprise the background so they can be removed from the foreground representation. To study the cortical computations supporting this process, we recorded single-unit activity in AC of male and female ferrets during the presentation of concurrent natural sounds from these two categories. In contrast to expectations from studies in high-order AC, single-unit responses to foreground sounds were strongly reduced relative to the paired background in primary and secondary AC. The degree of reduction could not be explained by a neuron's preference for the foreground or background stimulus in isolation but could be partially explained by spectrotemporal statistics that distinguish foreground and background categories. Responses to synthesized sounds with statistics either matched or randomized relative to natural sounds showed progressively decreased reduction of foreground responses as natural sound statistics were removed. These results challenge the expectation that cortical foreground representations emerge directly from a mixed representation in the auditory periphery. Instead, they suggest the early AC maintains a robust representation of background noise. Strong background representations may produce a distributed code, facilitating selection of foreground signals from a relatively small subpopulation of AC neurons at later processing stages.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4000,"publicationDate":"2025-03-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11884389/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/JNEUROSCI.0121-24.2024","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

In everyday hearing, listeners face the challenge of understanding behaviorally relevant foreground stimuli (speech, vocalizations) in complex backgrounds (environmental, mechanical noise). Prior studies have shown that high-order areas of human auditory cortex (AC) preattentively form an enhanced representation of foreground stimuli in the presence of background noise. This enhancement requires identifying and grouping the features that comprise the background so they can be removed from the foreground representation. To study the cortical computations supporting this process, we recorded single-unit activity in AC of male and female ferrets during the presentation of concurrent natural sounds from these two categories. In contrast to expectations from studies in high-order AC, single-unit responses to foreground sounds were strongly reduced relative to the paired background in primary and secondary AC. The degree of reduction could not be explained by a neuron's preference for the foreground or background stimulus in isolation but could be partially explained by spectrotemporal statistics that distinguish foreground and background categories. Responses to synthesized sounds with statistics either matched or randomized relative to natural sounds showed progressively decreased reduction of foreground responses as natural sound statistics were removed. These results challenge the expectation that cortical foreground representations emerge directly from a mixed representation in the auditory periphery. Instead, they suggest the early AC maintains a robust representation of background noise. Strong background representations may produce a distributed code, facilitating selection of foreground signals from a relatively small subpopulation of AC neurons at later processing stages.

听觉皮层对自然前景声音和背景声音的神经反应减少。
在日常听力中,听者面临着理解复杂背景(环境、机械噪音)中与行为相关的前景刺激(言语、发声)的挑战。先前的研究表明,在背景噪声存在的情况下,人类听觉皮层(AC)的高阶区域会形成对前景刺激的增强表征。这种增强需要识别和分组组成背景的特征,以便它们可以从前景表示中删除。为了研究支持这一过程的皮质计算,我们记录了雄性和雌性雪貂在同时呈现这两类自然声音时AC的单个单位活动。与高阶交流研究的预期相反,相对于配对背景,初级和次级交流中对前景声音的单单元反应大大减少。这种减少的程度不能用神经元对孤立的前景或背景刺激的偏好来解释,但可以部分解释为区分前景和背景类别的光谱时间统计。对与自然声音相匹配或随机化的合成声音的响应显示,随着自然声音统计数据的移除,前景响应的减少程度逐渐降低。这些结果挑战了皮层前景表征直接来自听觉外围的混合表征的预期。相反,他们认为早期的AC保持了对背景噪声的强大表征。强背景表示可以产生分布式代码,便于在后期处理阶段从相对较小的交流神经元亚群中选择前景信号。在一个充满竞争背景噪音的世界中感知重要的声音需要区分相关和不相关声源的能力。大多数先前研究这种背景/前景对比的神经机制的工作都支持听觉皮层活动在很大程度上不受背景噪音影响的理论,这与行为研究的证据一致。然而,目前尚不清楚背景噪声的哪些信息是在单单位水平上表示的。在这里,与主流理论相反,我们展示了雪貂听觉皮层对自然背景噪音的单一单元反应相对于对自然前景声音的反应占主导地位。在听觉皮层的早期阶段,背景噪声的鲁棒表征可能是将特征分组为感知对象和从前景信号中选择信息以在下游脑区域优先表征所必需的。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Journal of Neuroscience
Journal of Neuroscience 医学-神经科学
CiteScore
9.30
自引率
3.80%
发文量
1164
审稿时长
12 months
期刊介绍: JNeurosci (ISSN 0270-6474) is an official journal of the Society for Neuroscience. It is published weekly by the Society, fifty weeks a year, one volume a year. JNeurosci publishes papers on a broad range of topics of general interest to those working on the nervous system. Authors now have an Open Choice option for their published articles
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信