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Effects of Syllable Rate on Neuro-Behavioral Synchronization Across Modalities: Brain Oscillations and Speech Productions

Considerable work suggests the dominant syllable rhythm of the acoustic envelope is remarkably similar across languages (∼4–5 Hz) and that oscillatory brain activity tracks these quasiperiodic rhythms to facilitate speech processing. However, whether this fundamental periodicity represents a common...

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Autores principales: He, Deling, Buder, Eugene H., Bidelman, Gavin M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MIT Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10205147/
https://www.ncbi.nlm.nih.gov/pubmed/37229510
http://dx.doi.org/10.1162/nol_a_00102
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author He, Deling
Buder, Eugene H.
Bidelman, Gavin M.
author_facet He, Deling
Buder, Eugene H.
Bidelman, Gavin M.
author_sort He, Deling
collection PubMed
description Considerable work suggests the dominant syllable rhythm of the acoustic envelope is remarkably similar across languages (∼4–5 Hz) and that oscillatory brain activity tracks these quasiperiodic rhythms to facilitate speech processing. However, whether this fundamental periodicity represents a common organizing principle in both auditory and motor systems involved in speech has not been explicitly tested. To evaluate relations between entrainment in the perceptual and production domains, we measured individuals’ (i) neuroacoustic tracking of the EEG to speech trains and their (ii) simultaneous and non-simultaneous productions synchronized to syllable rates between 2.5 and 8.5 Hz. Productions made without concurrent auditory presentation isolated motor speech functions more purely. We show that neural synchronization flexibly adapts to the heard stimuli in a rate-dependent manner, but that phase locking is boosted near ∼4.5 Hz, the purported dominant rate of speech. Cued speech productions (recruit sensorimotor interaction) were optimal between 2.5 and 4.5 Hz, suggesting a low-frequency constraint on motor output and/or sensorimotor integration. In contrast, “pure” motor productions (without concurrent sound cues) were most precisely generated at rates of 4.5 and 5.5 Hz, paralleling the neuroacoustic data. Correlations further revealed strong links between receptive (EEG) and production synchronization abilities; individuals with stronger auditory-perceptual entrainment better matched speech rhythms motorically. Together, our findings support an intimate link between exogenous and endogenous rhythmic processing that is optimized at 4–5 Hz in both auditory and motor systems. Parallels across modalities could result from dynamics of the speech motor system coupled with experience-dependent tuning of the perceptual system via the sensorimotor interface.
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spelling pubmed-102051472023-05-24 Effects of Syllable Rate on Neuro-Behavioral Synchronization Across Modalities: Brain Oscillations and Speech Productions He, Deling Buder, Eugene H. Bidelman, Gavin M. Neurobiol Lang (Camb) Research Article Considerable work suggests the dominant syllable rhythm of the acoustic envelope is remarkably similar across languages (∼4–5 Hz) and that oscillatory brain activity tracks these quasiperiodic rhythms to facilitate speech processing. However, whether this fundamental periodicity represents a common organizing principle in both auditory and motor systems involved in speech has not been explicitly tested. To evaluate relations between entrainment in the perceptual and production domains, we measured individuals’ (i) neuroacoustic tracking of the EEG to speech trains and their (ii) simultaneous and non-simultaneous productions synchronized to syllable rates between 2.5 and 8.5 Hz. Productions made without concurrent auditory presentation isolated motor speech functions more purely. We show that neural synchronization flexibly adapts to the heard stimuli in a rate-dependent manner, but that phase locking is boosted near ∼4.5 Hz, the purported dominant rate of speech. Cued speech productions (recruit sensorimotor interaction) were optimal between 2.5 and 4.5 Hz, suggesting a low-frequency constraint on motor output and/or sensorimotor integration. In contrast, “pure” motor productions (without concurrent sound cues) were most precisely generated at rates of 4.5 and 5.5 Hz, paralleling the neuroacoustic data. Correlations further revealed strong links between receptive (EEG) and production synchronization abilities; individuals with stronger auditory-perceptual entrainment better matched speech rhythms motorically. Together, our findings support an intimate link between exogenous and endogenous rhythmic processing that is optimized at 4–5 Hz in both auditory and motor systems. Parallels across modalities could result from dynamics of the speech motor system coupled with experience-dependent tuning of the perceptual system via the sensorimotor interface. MIT Press 2023-05-11 /pmc/articles/PMC10205147/ /pubmed/37229510 http://dx.doi.org/10.1162/nol_a_00102 Text en © 2023 Massachusetts Institute of Technology 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 the original work is properly cited. For a full description of the license, please visit https://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
He, Deling
Buder, Eugene H.
Bidelman, Gavin M.
Effects of Syllable Rate on Neuro-Behavioral Synchronization Across Modalities: Brain Oscillations and Speech Productions
title Effects of Syllable Rate on Neuro-Behavioral Synchronization Across Modalities: Brain Oscillations and Speech Productions
title_full Effects of Syllable Rate on Neuro-Behavioral Synchronization Across Modalities: Brain Oscillations and Speech Productions
title_fullStr Effects of Syllable Rate on Neuro-Behavioral Synchronization Across Modalities: Brain Oscillations and Speech Productions
title_full_unstemmed Effects of Syllable Rate on Neuro-Behavioral Synchronization Across Modalities: Brain Oscillations and Speech Productions
title_short Effects of Syllable Rate on Neuro-Behavioral Synchronization Across Modalities: Brain Oscillations and Speech Productions
title_sort effects of syllable rate on neuro-behavioral synchronization across modalities: brain oscillations and speech productions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10205147/
https://www.ncbi.nlm.nih.gov/pubmed/37229510
http://dx.doi.org/10.1162/nol_a_00102
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