Gamma and theta/alpha-band oscillations in the electroencephalogram distinguish the content of inner speech.

IF 2.7 3区 医学 Q3 NEUROSCIENCES
eNeuro Pub Date : 2025-01-22 DOI:10.1523/ENEURO.0297-24.2025
Thomas J Whitford, Kevin M Spencer, Marianthe Godwin, Yoji Hirano, Lawrence Kin-Hei Chung, Wadim Vodovozov, Oren Griffiths, Anthony W F Harris, Mike E Le Pelley, Bradley N Jack
{"title":"Gamma and theta/alpha-band oscillations in the electroencephalogram distinguish the content of inner speech.","authors":"Thomas J Whitford, Kevin M Spencer, Marianthe Godwin, Yoji Hirano, Lawrence Kin-Hei Chung, Wadim Vodovozov, Oren Griffiths, Anthony W F Harris, Mike E Le Pelley, Bradley N Jack","doi":"10.1523/ENEURO.0297-24.2025","DOIUrl":null,"url":null,"abstract":"<p><p>Inner speech refers to the silent production of language in one's mind. As a purely mental action without obvious physical manifestations, inner speech has been notoriously difficult to quantify. Inner speech is thought to be closely related to overt speech. Overt speech has been consistently shown to elicit reduced auditory-evoked potentials compared to externally-generated speech (a phenomenon known as speaking-induced suppression), as well as changes in oscillatory activity in the gamma and theta frequency bands. Given the functional similarities between inner and overt speech, the present study used a novel experimental protocol to investigate whether these metrics can be used to distinguish the content of a person's inner speech. Healthy control participants (n = 129) produced an inner syllable at a precisely specified time. An audible syllable was concurrently presented which either matched or mismatched the content of the inner syllable. The N1 component of the auditory evoked potential was suppressed in the Match condition while the P2 component was suppressed in the Mismatch condition, replicating our previous findings. A novel finding was that the Match and Mismatch conditions could be differentiated on the basis of their evoked gamma and theta / alpha oscillations. There was a single gamma-band oscillation in the vicinity of the P2 that differed in spectral power between the Match and Mismatch conditions, which provides support for the idea that 'late' gamma-band activity may index consciously-perceived expectancy violations, or cognitive prediction errors. The Match and Mismatch conditions also differed in terms of their evoked power in a temporally-extended cluster which spanned the theta and alpha bands. The results of this study provide support for the phenomenon of 'inner speaking-induced suppression', and demonstrate that inner syllables can be differentiated using scalp electroencephalography (evoked potentials and oscillations) based on whether their content matches that of a simultaneously-presented audible syllable.<b>Significance statement</b> Inner speech refers to the silent production of language in one's mind. As a purely mental action without obvious physical manifestations, inner speech has been notoriously difficult to quantify empirically. The aim of the present study was to develop an objective, electroencephalography-based marker of inner speech that was sensitive to its content. The results of this study demonstrate that it is possible to distinguish between two syllables produced in inner speech on the basis of their auditory-evoked activity and evoked oscillations in the gamma and theta/alpha bands in the electroencephalogram. The gamma-band oscillation may represent a 'cognitive' prediction error. The ability to determine the content of a person's inner speech on the basis of a non-invasive biometric signal could have significant commercial, industrial, and clinical applications.</p>","PeriodicalId":11617,"journal":{"name":"eNeuro","volume":" ","pages":""},"PeriodicalIF":2.7000,"publicationDate":"2025-01-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"eNeuro","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/ENEURO.0297-24.2025","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Inner speech refers to the silent production of language in one's mind. As a purely mental action without obvious physical manifestations, inner speech has been notoriously difficult to quantify. Inner speech is thought to be closely related to overt speech. Overt speech has been consistently shown to elicit reduced auditory-evoked potentials compared to externally-generated speech (a phenomenon known as speaking-induced suppression), as well as changes in oscillatory activity in the gamma and theta frequency bands. Given the functional similarities between inner and overt speech, the present study used a novel experimental protocol to investigate whether these metrics can be used to distinguish the content of a person's inner speech. Healthy control participants (n = 129) produced an inner syllable at a precisely specified time. An audible syllable was concurrently presented which either matched or mismatched the content of the inner syllable. The N1 component of the auditory evoked potential was suppressed in the Match condition while the P2 component was suppressed in the Mismatch condition, replicating our previous findings. A novel finding was that the Match and Mismatch conditions could be differentiated on the basis of their evoked gamma and theta / alpha oscillations. There was a single gamma-band oscillation in the vicinity of the P2 that differed in spectral power between the Match and Mismatch conditions, which provides support for the idea that 'late' gamma-band activity may index consciously-perceived expectancy violations, or cognitive prediction errors. The Match and Mismatch conditions also differed in terms of their evoked power in a temporally-extended cluster which spanned the theta and alpha bands. The results of this study provide support for the phenomenon of 'inner speaking-induced suppression', and demonstrate that inner syllables can be differentiated using scalp electroencephalography (evoked potentials and oscillations) based on whether their content matches that of a simultaneously-presented audible syllable.Significance statement Inner speech refers to the silent production of language in one's mind. As a purely mental action without obvious physical manifestations, inner speech has been notoriously difficult to quantify empirically. The aim of the present study was to develop an objective, electroencephalography-based marker of inner speech that was sensitive to its content. The results of this study demonstrate that it is possible to distinguish between two syllables produced in inner speech on the basis of their auditory-evoked activity and evoked oscillations in the gamma and theta/alpha bands in the electroencephalogram. The gamma-band oscillation may represent a 'cognitive' prediction error. The ability to determine the content of a person's inner speech on the basis of a non-invasive biometric signal could have significant commercial, industrial, and clinical applications.

求助全文
约1分钟内获得全文 求助全文
来源期刊
eNeuro
eNeuro Neuroscience-General Neuroscience
CiteScore
5.00
自引率
2.90%
发文量
486
审稿时长
16 weeks
期刊介绍: An open-access journal from the Society for Neuroscience, eNeuro publishes high-quality, broad-based, peer-reviewed research focused solely on the field of neuroscience. eNeuro embodies an emerging scientific vision that offers a new experience for authors and readers, all in support of the Society’s mission to advance understanding of the brain and nervous system.
×
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