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Impaired Speaking-Induced Suppression in Alzheimer’s Disease

Alzheimer’s disease (AD) is a neurodegenerative disease involving cognitive impairment and abnormalities in speech and language. Here, we examine how AD affects the fidelity of auditory feedback predictions during speaking. We focus on the phenomenon of speaking-induced suppression (SIS), the audito...

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Autores principales: Kim, Kyunghee X., Dale, Corby L., Ranasinghe, Kamalini G., Kothare, Hardik, Beagle, Alexander J., Lerner, Hannah, Mizuiri, Danielle, Gorno-Tempini, Maria Luisa, Vossel, Keith, Nagarajan, Srikantan S., Houde, John F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10249944/
https://www.ncbi.nlm.nih.gov/pubmed/37221089
http://dx.doi.org/10.1523/ENEURO.0056-23.2023
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author Kim, Kyunghee X.
Dale, Corby L.
Ranasinghe, Kamalini G.
Kothare, Hardik
Beagle, Alexander J.
Lerner, Hannah
Mizuiri, Danielle
Gorno-Tempini, Maria Luisa
Vossel, Keith
Nagarajan, Srikantan S.
Houde, John F.
author_facet Kim, Kyunghee X.
Dale, Corby L.
Ranasinghe, Kamalini G.
Kothare, Hardik
Beagle, Alexander J.
Lerner, Hannah
Mizuiri, Danielle
Gorno-Tempini, Maria Luisa
Vossel, Keith
Nagarajan, Srikantan S.
Houde, John F.
author_sort Kim, Kyunghee X.
collection PubMed
description Alzheimer’s disease (AD) is a neurodegenerative disease involving cognitive impairment and abnormalities in speech and language. Here, we examine how AD affects the fidelity of auditory feedback predictions during speaking. We focus on the phenomenon of speaking-induced suppression (SIS), the auditory cortical responses’ suppression during auditory feedback processing. SIS is determined by subtracting the magnitude of auditory cortical responses during speaking from listening to playback of the same speech. Our state feedback control (SFC) model of speech motor control explains SIS as arising from the onset of auditory feedback matching a prediction of that feedback onset during speaking, a prediction that is absent during passive listening to playback of the auditory feedback. Our model hypothesizes that the auditory cortical response to auditory feedback reflects the mismatch with the prediction: small during speaking, large during listening, with the difference being SIS. Normally, during speaking, auditory feedback matches its predictions, then SIS will be large. Any reductions in SIS will indicate inaccuracy in auditory feedback prediction not matching the actual feedback. We investigated SIS in AD patients [n = 20; mean (SD) age, 60.77 (10.04); female (%), 55.00] and healthy controls [n = 12; mean (SD) age, 63.68 (6.07); female (%), 83.33] through magnetoencephalography (MEG)-based functional imaging. We found a significant reduction in SIS at ∼100 ms in AD patients compared with healthy controls (linear mixed effects model, F((1,57.5)) = 6.849, p = 0.011). The results suggest that AD patients generate inaccurate auditory feedback predictions, contributing to abnormalities in AD speech.
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spelling pubmed-102499442023-06-09 Impaired Speaking-Induced Suppression in Alzheimer’s Disease Kim, Kyunghee X. Dale, Corby L. Ranasinghe, Kamalini G. Kothare, Hardik Beagle, Alexander J. Lerner, Hannah Mizuiri, Danielle Gorno-Tempini, Maria Luisa Vossel, Keith Nagarajan, Srikantan S. Houde, John F. eNeuro Research Article: New Research Alzheimer’s disease (AD) is a neurodegenerative disease involving cognitive impairment and abnormalities in speech and language. Here, we examine how AD affects the fidelity of auditory feedback predictions during speaking. We focus on the phenomenon of speaking-induced suppression (SIS), the auditory cortical responses’ suppression during auditory feedback processing. SIS is determined by subtracting the magnitude of auditory cortical responses during speaking from listening to playback of the same speech. Our state feedback control (SFC) model of speech motor control explains SIS as arising from the onset of auditory feedback matching a prediction of that feedback onset during speaking, a prediction that is absent during passive listening to playback of the auditory feedback. Our model hypothesizes that the auditory cortical response to auditory feedback reflects the mismatch with the prediction: small during speaking, large during listening, with the difference being SIS. Normally, during speaking, auditory feedback matches its predictions, then SIS will be large. Any reductions in SIS will indicate inaccuracy in auditory feedback prediction not matching the actual feedback. We investigated SIS in AD patients [n = 20; mean (SD) age, 60.77 (10.04); female (%), 55.00] and healthy controls [n = 12; mean (SD) age, 63.68 (6.07); female (%), 83.33] through magnetoencephalography (MEG)-based functional imaging. We found a significant reduction in SIS at ∼100 ms in AD patients compared with healthy controls (linear mixed effects model, F((1,57.5)) = 6.849, p = 0.011). The results suggest that AD patients generate inaccurate auditory feedback predictions, contributing to abnormalities in AD speech. Society for Neuroscience 2023-06-05 /pmc/articles/PMC10249944/ /pubmed/37221089 http://dx.doi.org/10.1523/ENEURO.0056-23.2023 Text en Copyright © 2023 Kim et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article: New Research
Kim, Kyunghee X.
Dale, Corby L.
Ranasinghe, Kamalini G.
Kothare, Hardik
Beagle, Alexander J.
Lerner, Hannah
Mizuiri, Danielle
Gorno-Tempini, Maria Luisa
Vossel, Keith
Nagarajan, Srikantan S.
Houde, John F.
Impaired Speaking-Induced Suppression in Alzheimer’s Disease
title Impaired Speaking-Induced Suppression in Alzheimer’s Disease
title_full Impaired Speaking-Induced Suppression in Alzheimer’s Disease
title_fullStr Impaired Speaking-Induced Suppression in Alzheimer’s Disease
title_full_unstemmed Impaired Speaking-Induced Suppression in Alzheimer’s Disease
title_short Impaired Speaking-Induced Suppression in Alzheimer’s Disease
title_sort impaired speaking-induced suppression in alzheimer’s disease
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10249944/
https://www.ncbi.nlm.nih.gov/pubmed/37221089
http://dx.doi.org/10.1523/ENEURO.0056-23.2023
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