Garret Lynn Kurteff, Alyssa M Field, Saman Asghar, Elizabeth C Tyler-Kabara, Dave Clarke, Howard L Weiner, Anne E Anderson, Andrew J Watrous, Robert J Buchanan, Pradeep N Modur, Liberty S Hamilton
{"title":"Spatiotemporal mapping of auditory onsets during speech production.","authors":"Garret Lynn Kurteff, Alyssa M Field, Saman Asghar, Elizabeth C Tyler-Kabara, Dave Clarke, Howard L Weiner, Anne E Anderson, Andrew J Watrous, Robert J Buchanan, Pradeep N Modur, Liberty S Hamilton","doi":"10.1523/JNEUROSCI.1109-24.2024","DOIUrl":null,"url":null,"abstract":"<p><p>The human auditory cortex is organized according to the timing and spectral characteristics of speech sounds during speech perception. During listening, the posterior superior temporal gyrus is organized according to onset responses, which segment acoustic boundaries in speech, and sustained responses, which further process phonological content. When we speak, the auditory system is actively processing the sound of our own voice to detect and correct speech errors in real time. This manifests in neural recordings as suppression of auditory responses during speech production compared to perception, but whether this differentially affects onset and sustained temporal profiles is not known. Here we investigated this question using intracranial EEG recorded from seventeen pediatric, adolescent, and adult patients with medication-resistant epilepsy while they performed a reading/listening task. We identified onset and sustained responses to speech in bilateral auditory cortex and observed a selective suppression of onset responses during speech production. We conclude that onset responses provide a temporal landmark during speech perception that is redundant with forward prediction during speech production and are therefore suppressed. Phonological feature tuning in these \"onset suppression\" electrodes remained stable between perception and production. Notably, auditory onset responses and phonological feature tuning were present in the posterior insula during both speech perception and production, suggesting an anatomically and functionally separate auditory processing zone that we believe to be involved in multisensory integration during speech perception and feedback control.<b>Significance Statement</b> Specific neural populations in the auditory cortex preferentially respond to the onset of speech sounds. These \"onset responses\" aid in perceiving boundaries in continuous speech. We recorded neural responses from patients with intracranial electrodes during a speaking and listening task to investigate the role of onset responses in speech production. Onset responses were present in the auditory cortex during listening, but absent during speaking. On the other hand, onset responses were observed in the insula during both conditions, suggesting a different functional role for the insula in auditory feedback processing. These findings extend our knowledge of how different parts of the brain involved in feedback control operate during speech production by identifying two functionally and anatomically distinct patterns of activity.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":null,"pages":null},"PeriodicalIF":4.4000,"publicationDate":"2024-10-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/JNEUROSCI.1109-24.2024","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
The human auditory cortex is organized according to the timing and spectral characteristics of speech sounds during speech perception. During listening, the posterior superior temporal gyrus is organized according to onset responses, which segment acoustic boundaries in speech, and sustained responses, which further process phonological content. When we speak, the auditory system is actively processing the sound of our own voice to detect and correct speech errors in real time. This manifests in neural recordings as suppression of auditory responses during speech production compared to perception, but whether this differentially affects onset and sustained temporal profiles is not known. Here we investigated this question using intracranial EEG recorded from seventeen pediatric, adolescent, and adult patients with medication-resistant epilepsy while they performed a reading/listening task. We identified onset and sustained responses to speech in bilateral auditory cortex and observed a selective suppression of onset responses during speech production. We conclude that onset responses provide a temporal landmark during speech perception that is redundant with forward prediction during speech production and are therefore suppressed. Phonological feature tuning in these "onset suppression" electrodes remained stable between perception and production. Notably, auditory onset responses and phonological feature tuning were present in the posterior insula during both speech perception and production, suggesting an anatomically and functionally separate auditory processing zone that we believe to be involved in multisensory integration during speech perception and feedback control.Significance Statement Specific neural populations in the auditory cortex preferentially respond to the onset of speech sounds. These "onset responses" aid in perceiving boundaries in continuous speech. We recorded neural responses from patients with intracranial electrodes during a speaking and listening task to investigate the role of onset responses in speech production. Onset responses were present in the auditory cortex during listening, but absent during speaking. On the other hand, onset responses were observed in the insula during both conditions, suggesting a different functional role for the insula in auditory feedback processing. These findings extend our knowledge of how different parts of the brain involved in feedback control operate during speech production by identifying two functionally and anatomically distinct patterns of activity.
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