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A cortical network processes auditory error signals during human speech production to maintain fluency

Hearing one’s own voice is critical for fluent speech production as it allows for the detection and correction of vocalization errors in real time. This behavior known as the auditory feedback control of speech is impaired in various neurological disorders ranging from stuttering to aphasia; however...

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Autores principales: Ozker, Muge, Doyle, Werner, Devinsky, Orrin, Flinker, Adeen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8812883/
https://www.ncbi.nlm.nih.gov/pubmed/35113857
http://dx.doi.org/10.1371/journal.pbio.3001493
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author Ozker, Muge
Doyle, Werner
Devinsky, Orrin
Flinker, Adeen
author_facet Ozker, Muge
Doyle, Werner
Devinsky, Orrin
Flinker, Adeen
author_sort Ozker, Muge
collection PubMed
description Hearing one’s own voice is critical for fluent speech production as it allows for the detection and correction of vocalization errors in real time. This behavior known as the auditory feedback control of speech is impaired in various neurological disorders ranging from stuttering to aphasia; however, the underlying neural mechanisms are still poorly understood. Computational models of speech motor control suggest that, during speech production, the brain uses an efference copy of the motor command to generate an internal estimate of the speech output. When actual feedback differs from this internal estimate, an error signal is generated to correct the internal estimate and update necessary motor commands to produce intended speech. We were able to localize the auditory error signal using electrocorticographic recordings from neurosurgical participants during a delayed auditory feedback (DAF) paradigm. In this task, participants hear their voice with a time delay as they produced words and sentences (similar to an echo on a conference call), which is well known to disrupt fluency by causing slow and stutter-like speech in humans. We observed a significant response enhancement in auditory cortex that scaled with the duration of feedback delay, indicating an auditory speech error signal. Immediately following auditory cortex, dorsal precentral gyrus (dPreCG), a region that has not been implicated in auditory feedback processing before, exhibited a markedly similar response enhancement, suggesting a tight coupling between the 2 regions. Critically, response enhancement in dPreCG occurred only during articulation of long utterances due to a continuous mismatch between produced speech and reafferent feedback. These results suggest that dPreCG plays an essential role in processing auditory error signals during speech production to maintain fluency.
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spelling pubmed-88128832022-02-04 A cortical network processes auditory error signals during human speech production to maintain fluency Ozker, Muge Doyle, Werner Devinsky, Orrin Flinker, Adeen PLoS Biol Research Article Hearing one’s own voice is critical for fluent speech production as it allows for the detection and correction of vocalization errors in real time. This behavior known as the auditory feedback control of speech is impaired in various neurological disorders ranging from stuttering to aphasia; however, the underlying neural mechanisms are still poorly understood. Computational models of speech motor control suggest that, during speech production, the brain uses an efference copy of the motor command to generate an internal estimate of the speech output. When actual feedback differs from this internal estimate, an error signal is generated to correct the internal estimate and update necessary motor commands to produce intended speech. We were able to localize the auditory error signal using electrocorticographic recordings from neurosurgical participants during a delayed auditory feedback (DAF) paradigm. In this task, participants hear their voice with a time delay as they produced words and sentences (similar to an echo on a conference call), which is well known to disrupt fluency by causing slow and stutter-like speech in humans. We observed a significant response enhancement in auditory cortex that scaled with the duration of feedback delay, indicating an auditory speech error signal. Immediately following auditory cortex, dorsal precentral gyrus (dPreCG), a region that has not been implicated in auditory feedback processing before, exhibited a markedly similar response enhancement, suggesting a tight coupling between the 2 regions. Critically, response enhancement in dPreCG occurred only during articulation of long utterances due to a continuous mismatch between produced speech and reafferent feedback. These results suggest that dPreCG plays an essential role in processing auditory error signals during speech production to maintain fluency. Public Library of Science 2022-02-03 /pmc/articles/PMC8812883/ /pubmed/35113857 http://dx.doi.org/10.1371/journal.pbio.3001493 Text en © 2022 Ozker et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ozker, Muge
Doyle, Werner
Devinsky, Orrin
Flinker, Adeen
A cortical network processes auditory error signals during human speech production to maintain fluency
title A cortical network processes auditory error signals during human speech production to maintain fluency
title_full A cortical network processes auditory error signals during human speech production to maintain fluency
title_fullStr A cortical network processes auditory error signals during human speech production to maintain fluency
title_full_unstemmed A cortical network processes auditory error signals during human speech production to maintain fluency
title_short A cortical network processes auditory error signals during human speech production to maintain fluency
title_sort cortical network processes auditory error signals during human speech production to maintain fluency
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8812883/
https://www.ncbi.nlm.nih.gov/pubmed/35113857
http://dx.doi.org/10.1371/journal.pbio.3001493
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