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Rhythmic modulation of prediction errors: A top-down gating role for the beta-range in speech processing
Natural speech perception requires processing the ongoing acoustic input while keeping in mind the preceding one and predicting the next. This complex computational problem could be handled by a dynamic multi-timescale hierarchical inferential process that coordinates the information flow up and dow...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10655987/ https://www.ncbi.nlm.nih.gov/pubmed/37934766 http://dx.doi.org/10.1371/journal.pcbi.1011595 |
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author | Hovsepyan, Sevada Olasagasti, Itsaso Giraud, Anne-Lise |
author_facet | Hovsepyan, Sevada Olasagasti, Itsaso Giraud, Anne-Lise |
author_sort | Hovsepyan, Sevada |
collection | PubMed |
description | Natural speech perception requires processing the ongoing acoustic input while keeping in mind the preceding one and predicting the next. This complex computational problem could be handled by a dynamic multi-timescale hierarchical inferential process that coordinates the information flow up and down the language network hierarchy. Using a predictive coding computational model (Precoss-β) that identifies online individual syllables from continuous speech, we address the advantage of a rhythmic modulation of up and down information flows, and whether beta oscillations could be optimal for this. In the model, and consistent with experimental data, theta and low-gamma neural frequency scales ensure syllable-tracking and phoneme-level speech encoding, respectively, while the beta rhythm is associated with inferential processes. We show that a rhythmic alternation of bottom-up and top-down processing regimes improves syllable recognition, and that optimal efficacy is reached when the alternation of bottom-up and top-down regimes, via oscillating prediction error precisions, is in the beta range (around 20–30 Hz). These results not only demonstrate the advantage of a rhythmic alternation of up- and down-going information, but also that the low-beta range is optimal given sensory analysis at theta and low-gamma scales. While specific to speech processing, the notion of alternating bottom-up and top-down processes with frequency multiplexing might generalize to other cognitive architectures. |
format | Online Article Text |
id | pubmed-10655987 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-106559872023-11-07 Rhythmic modulation of prediction errors: A top-down gating role for the beta-range in speech processing Hovsepyan, Sevada Olasagasti, Itsaso Giraud, Anne-Lise PLoS Comput Biol Research Article Natural speech perception requires processing the ongoing acoustic input while keeping in mind the preceding one and predicting the next. This complex computational problem could be handled by a dynamic multi-timescale hierarchical inferential process that coordinates the information flow up and down the language network hierarchy. Using a predictive coding computational model (Precoss-β) that identifies online individual syllables from continuous speech, we address the advantage of a rhythmic modulation of up and down information flows, and whether beta oscillations could be optimal for this. In the model, and consistent with experimental data, theta and low-gamma neural frequency scales ensure syllable-tracking and phoneme-level speech encoding, respectively, while the beta rhythm is associated with inferential processes. We show that a rhythmic alternation of bottom-up and top-down processing regimes improves syllable recognition, and that optimal efficacy is reached when the alternation of bottom-up and top-down regimes, via oscillating prediction error precisions, is in the beta range (around 20–30 Hz). These results not only demonstrate the advantage of a rhythmic alternation of up- and down-going information, but also that the low-beta range is optimal given sensory analysis at theta and low-gamma scales. While specific to speech processing, the notion of alternating bottom-up and top-down processes with frequency multiplexing might generalize to other cognitive architectures. Public Library of Science 2023-11-07 /pmc/articles/PMC10655987/ /pubmed/37934766 http://dx.doi.org/10.1371/journal.pcbi.1011595 Text en © 2023 Hovsepyan 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 Hovsepyan, Sevada Olasagasti, Itsaso Giraud, Anne-Lise Rhythmic modulation of prediction errors: A top-down gating role for the beta-range in speech processing |
title | Rhythmic modulation of prediction errors: A top-down gating role for the beta-range in speech processing |
title_full | Rhythmic modulation of prediction errors: A top-down gating role for the beta-range in speech processing |
title_fullStr | Rhythmic modulation of prediction errors: A top-down gating role for the beta-range in speech processing |
title_full_unstemmed | Rhythmic modulation of prediction errors: A top-down gating role for the beta-range in speech processing |
title_short | Rhythmic modulation of prediction errors: A top-down gating role for the beta-range in speech processing |
title_sort | rhythmic modulation of prediction errors: a top-down gating role for the beta-range in speech processing |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10655987/ https://www.ncbi.nlm.nih.gov/pubmed/37934766 http://dx.doi.org/10.1371/journal.pcbi.1011595 |
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