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Spectral-temporal EEG dynamics of speech discrimination processing in infants during sleep

BACKGROUND: Oddball paradigms are frequently used to study auditory discrimination by comparing event-related potential (ERP) responses from a standard, high probability sound and to a deviant, low probability sound. Previous research has established that such paradigms, such as the mismatch respons...

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Autores principales: Gilley, Phillip M., Uhler, Kristin, Watson, Kaylee, Yoshinaga-Itano, Christine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5439120/
https://www.ncbi.nlm.nih.gov/pubmed/28330464
http://dx.doi.org/10.1186/s12868-017-0353-4
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author Gilley, Phillip M.
Uhler, Kristin
Watson, Kaylee
Yoshinaga-Itano, Christine
author_facet Gilley, Phillip M.
Uhler, Kristin
Watson, Kaylee
Yoshinaga-Itano, Christine
author_sort Gilley, Phillip M.
collection PubMed
description BACKGROUND: Oddball paradigms are frequently used to study auditory discrimination by comparing event-related potential (ERP) responses from a standard, high probability sound and to a deviant, low probability sound. Previous research has established that such paradigms, such as the mismatch response or mismatch negativity, are useful for examining auditory processes in young children and infants across various sleep and attention states. The extent to which oddball ERP responses may reflect subtle discrimination effects, such as speech discrimination, is largely unknown, especially in infants that have not yet acquired speech and language. RESULTS: Mismatch responses for three contrasts (non-speech, vowel, and consonant) were computed as a spectral-temporal probability function in 24 infants, and analyzed at the group level by a modified multidimensional scaling. Immediately following an onset gamma response (30–50 Hz), the emergence of a beta oscillation (12–30 Hz) was temporally coupled with a lower frequency theta oscillation (2–8 Hz). The spectral-temporal probability of this coupling effect relative to a subsequent theta modulation corresponds with discrimination difficulty for non-speech, vowel, and consonant contrast features. DISCUSSION: The theta modulation effect suggests that unexpected sounds are encoded as a probabilistic measure of surprise. These results support the notion that auditory discrimination is driven by the development of brain networks for predictive processing, and can be measured in infants during sleep. The results presented here have implications for the interpretation of discrimination as a probabilistic process, and may provide a basis for the development of single-subject and single-trial classification in a clinically useful context. CONCLUSION: An infant’s brain is processing information about the environment and performing computations, even during sleep. These computations reflect subtle differences in acoustic feature processing that are necessary for language-learning. Results from this study suggest that brain responses to deviant sounds in an oddball paradigm follow a cascade of oscillatory modulations. This cascade begins with a gamma response that later emerges as a beta synchronization, which is temporally coupled with a theta modulation, and followed by a second, subsequent theta modulation. The difference in frequency and timing of the theta modulations appears to reflect a measure of surprise. These insights into the neurophysiological mechanisms of auditory discrimination provide a basis for exploring the clinically utility of the MMR (TF) and other auditory oddball responses.
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spelling pubmed-54391202017-05-23 Spectral-temporal EEG dynamics of speech discrimination processing in infants during sleep Gilley, Phillip M. Uhler, Kristin Watson, Kaylee Yoshinaga-Itano, Christine BMC Neurosci Research Article BACKGROUND: Oddball paradigms are frequently used to study auditory discrimination by comparing event-related potential (ERP) responses from a standard, high probability sound and to a deviant, low probability sound. Previous research has established that such paradigms, such as the mismatch response or mismatch negativity, are useful for examining auditory processes in young children and infants across various sleep and attention states. The extent to which oddball ERP responses may reflect subtle discrimination effects, such as speech discrimination, is largely unknown, especially in infants that have not yet acquired speech and language. RESULTS: Mismatch responses for three contrasts (non-speech, vowel, and consonant) were computed as a spectral-temporal probability function in 24 infants, and analyzed at the group level by a modified multidimensional scaling. Immediately following an onset gamma response (30–50 Hz), the emergence of a beta oscillation (12–30 Hz) was temporally coupled with a lower frequency theta oscillation (2–8 Hz). The spectral-temporal probability of this coupling effect relative to a subsequent theta modulation corresponds with discrimination difficulty for non-speech, vowel, and consonant contrast features. DISCUSSION: The theta modulation effect suggests that unexpected sounds are encoded as a probabilistic measure of surprise. These results support the notion that auditory discrimination is driven by the development of brain networks for predictive processing, and can be measured in infants during sleep. The results presented here have implications for the interpretation of discrimination as a probabilistic process, and may provide a basis for the development of single-subject and single-trial classification in a clinically useful context. CONCLUSION: An infant’s brain is processing information about the environment and performing computations, even during sleep. These computations reflect subtle differences in acoustic feature processing that are necessary for language-learning. Results from this study suggest that brain responses to deviant sounds in an oddball paradigm follow a cascade of oscillatory modulations. This cascade begins with a gamma response that later emerges as a beta synchronization, which is temporally coupled with a theta modulation, and followed by a second, subsequent theta modulation. The difference in frequency and timing of the theta modulations appears to reflect a measure of surprise. These insights into the neurophysiological mechanisms of auditory discrimination provide a basis for exploring the clinically utility of the MMR (TF) and other auditory oddball responses. BioMed Central 2017-03-22 /pmc/articles/PMC5439120/ /pubmed/28330464 http://dx.doi.org/10.1186/s12868-017-0353-4 Text en © The Author(s) 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Gilley, Phillip M.
Uhler, Kristin
Watson, Kaylee
Yoshinaga-Itano, Christine
Spectral-temporal EEG dynamics of speech discrimination processing in infants during sleep
title Spectral-temporal EEG dynamics of speech discrimination processing in infants during sleep
title_full Spectral-temporal EEG dynamics of speech discrimination processing in infants during sleep
title_fullStr Spectral-temporal EEG dynamics of speech discrimination processing in infants during sleep
title_full_unstemmed Spectral-temporal EEG dynamics of speech discrimination processing in infants during sleep
title_short Spectral-temporal EEG dynamics of speech discrimination processing in infants during sleep
title_sort spectral-temporal eeg dynamics of speech discrimination processing in infants during sleep
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5439120/
https://www.ncbi.nlm.nih.gov/pubmed/28330464
http://dx.doi.org/10.1186/s12868-017-0353-4
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