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The Time Course of Language Production as Revealed by Pattern Classification of MEG Sensor Data

Language production involves a complex set of computations, from conceptualization to articulation, which are thought to engage cascading neural events in the language network. However, recent neuromagnetic evidence suggests simultaneous meaning-to-speech mapping in picture naming tasks, as indexed...

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Autores principales: Carota, Francesca, Schoffelen, Jan-Mathijs, Oostenveld, Robert, Indefrey, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9302460/
https://www.ncbi.nlm.nih.gov/pubmed/35680410
http://dx.doi.org/10.1523/JNEUROSCI.1923-21.2022
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author Carota, Francesca
Schoffelen, Jan-Mathijs
Oostenveld, Robert
Indefrey, Peter
author_facet Carota, Francesca
Schoffelen, Jan-Mathijs
Oostenveld, Robert
Indefrey, Peter
author_sort Carota, Francesca
collection PubMed
description Language production involves a complex set of computations, from conceptualization to articulation, which are thought to engage cascading neural events in the language network. However, recent neuromagnetic evidence suggests simultaneous meaning-to-speech mapping in picture naming tasks, as indexed by early parallel activation of frontotemporal regions to lexical semantic, phonological, and articulatory information. Here we investigate the time course of word production, asking to what extent such “earliness” is a distinctive property of the associated spatiotemporal dynamics. Using MEG, we recorded the neural signals of 34 human subjects (26 males) overtly naming 134 images from four semantic object categories (animals, foods, tools, clothes). Within each category, we covaried word length, as quantified by the number of syllables contained in a word, and phonological neighborhood density to target lexical and post-lexical phonological/phonetic processes. Multivariate pattern analyses searchlights in sensor space distinguished the stimulus-locked spatiotemporal responses to object categories early on, from 150 to 250 ms after picture onset, whereas word length was decoded in left frontotemporal sensors at 250-350 ms, followed by the latency of phonological neighborhood density (350-450 ms). Our results suggest a progression of neural activity from posterior to anterior language regions for the semantic and phonological/phonetic computations preparing overt speech, thus supporting serial cascading models of word production. SIGNIFICANCE STATEMENT Current psycholinguistic models make divergent predictions on how a preverbal message is mapped onto articulatory output during the language planning. Serial models predict a cascading sequence of hierarchically organized neural computations from conceptualization to articulation. In contrast, parallel models posit early simultaneous activation of multiple conceptual, phonological, and articulatory information in the language system. Here we asked whether such earliness is a distinctive property of the neural dynamics of word production. The combination of the millisecond precision of MEG with multivariate pattern analyses revealed subsequent onset times for the neural events supporting semantic and phonological/phonetic operations, progressing from posterior occipitotemporal to frontal sensor areas. The findings bring new insights for refining current theories of language production.
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spelling pubmed-93024602022-08-01 The Time Course of Language Production as Revealed by Pattern Classification of MEG Sensor Data Carota, Francesca Schoffelen, Jan-Mathijs Oostenveld, Robert Indefrey, Peter J Neurosci Research Articles Language production involves a complex set of computations, from conceptualization to articulation, which are thought to engage cascading neural events in the language network. However, recent neuromagnetic evidence suggests simultaneous meaning-to-speech mapping in picture naming tasks, as indexed by early parallel activation of frontotemporal regions to lexical semantic, phonological, and articulatory information. Here we investigate the time course of word production, asking to what extent such “earliness” is a distinctive property of the associated spatiotemporal dynamics. Using MEG, we recorded the neural signals of 34 human subjects (26 males) overtly naming 134 images from four semantic object categories (animals, foods, tools, clothes). Within each category, we covaried word length, as quantified by the number of syllables contained in a word, and phonological neighborhood density to target lexical and post-lexical phonological/phonetic processes. Multivariate pattern analyses searchlights in sensor space distinguished the stimulus-locked spatiotemporal responses to object categories early on, from 150 to 250 ms after picture onset, whereas word length was decoded in left frontotemporal sensors at 250-350 ms, followed by the latency of phonological neighborhood density (350-450 ms). Our results suggest a progression of neural activity from posterior to anterior language regions for the semantic and phonological/phonetic computations preparing overt speech, thus supporting serial cascading models of word production. SIGNIFICANCE STATEMENT Current psycholinguistic models make divergent predictions on how a preverbal message is mapped onto articulatory output during the language planning. Serial models predict a cascading sequence of hierarchically organized neural computations from conceptualization to articulation. In contrast, parallel models posit early simultaneous activation of multiple conceptual, phonological, and articulatory information in the language system. Here we asked whether such earliness is a distinctive property of the neural dynamics of word production. The combination of the millisecond precision of MEG with multivariate pattern analyses revealed subsequent onset times for the neural events supporting semantic and phonological/phonetic operations, progressing from posterior occipitotemporal to frontal sensor areas. The findings bring new insights for refining current theories of language production. Society for Neuroscience 2022-07-20 /pmc/articles/PMC9302460/ /pubmed/35680410 http://dx.doi.org/10.1523/JNEUROSCI.1923-21.2022 Text en Copyright © 2022 Carota 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 Articles
Carota, Francesca
Schoffelen, Jan-Mathijs
Oostenveld, Robert
Indefrey, Peter
The Time Course of Language Production as Revealed by Pattern Classification of MEG Sensor Data
title The Time Course of Language Production as Revealed by Pattern Classification of MEG Sensor Data
title_full The Time Course of Language Production as Revealed by Pattern Classification of MEG Sensor Data
title_fullStr The Time Course of Language Production as Revealed by Pattern Classification of MEG Sensor Data
title_full_unstemmed The Time Course of Language Production as Revealed by Pattern Classification of MEG Sensor Data
title_short The Time Course of Language Production as Revealed by Pattern Classification of MEG Sensor Data
title_sort time course of language production as revealed by pattern classification of meg sensor data
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9302460/
https://www.ncbi.nlm.nih.gov/pubmed/35680410
http://dx.doi.org/10.1523/JNEUROSCI.1923-21.2022
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