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Lateralization and Time-Course of Cortical Phonological Representations during Syllable Production

Spoken language contains information at a broad range of timescales, from phonetic distinctions on the order of milliseconds to semantic contexts which shift over seconds to minutes. It is not well understood how the brain’s speech production systems combine features at these timescales into a coher...

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Autores principales: Meier, Andrew, Kuzdeba, Scott, Jackson, Liam, Daliri, Ayoub, Tourville, Jason A., Guenther, Frank H., Greenlee, Jeremy D. W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10561542/
https://www.ncbi.nlm.nih.gov/pubmed/37739786
http://dx.doi.org/10.1523/ENEURO.0474-22.2023
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author Meier, Andrew
Kuzdeba, Scott
Jackson, Liam
Daliri, Ayoub
Tourville, Jason A.
Guenther, Frank H.
Greenlee, Jeremy D. W.
author_facet Meier, Andrew
Kuzdeba, Scott
Jackson, Liam
Daliri, Ayoub
Tourville, Jason A.
Guenther, Frank H.
Greenlee, Jeremy D. W.
author_sort Meier, Andrew
collection PubMed
description Spoken language contains information at a broad range of timescales, from phonetic distinctions on the order of milliseconds to semantic contexts which shift over seconds to minutes. It is not well understood how the brain’s speech production systems combine features at these timescales into a coherent vocal output. We investigated the spatial and temporal representations in cerebral cortex of three phonological units with different durations: consonants, vowels, and syllables. Electrocorticography (ECoG) recordings were obtained from five participants while speaking single syllables. We developed a novel clustering and Kalman filter-based trend analysis procedure to sort electrodes into temporal response profiles. A linear discriminant classifier was used to determine how strongly each electrode’s response encoded phonological features. We found distinct time-courses of encoding phonological units depending on their duration: consonants were represented more during speech preparation, vowels were represented evenly throughout trials, and syllables during production. Locations of strongly speech-encoding electrodes (the top 30% of electrodes) likewise depended on phonological element duration, with consonant-encoding electrodes left-lateralized, vowel-encoding hemispherically balanced, and syllable-encoding right-lateralized. The lateralization of speech-encoding electrodes depended on onset time, with electrodes active before or after speech production favoring left hemisphere and those active during speech favoring the right. Single-electrode speech classification revealed cortical areas with preferential encoding of particular phonemic elements, including consonant encoding in the left precentral and postcentral gyri and syllable encoding in the right middle frontal gyrus. Our findings support neurolinguistic theories of left hemisphere specialization for processing short-timescale linguistic units and right hemisphere processing of longer-duration units.
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spelling pubmed-105615422023-10-10 Lateralization and Time-Course of Cortical Phonological Representations during Syllable Production Meier, Andrew Kuzdeba, Scott Jackson, Liam Daliri, Ayoub Tourville, Jason A. Guenther, Frank H. Greenlee, Jeremy D. W. eNeuro Research Article: New Research Spoken language contains information at a broad range of timescales, from phonetic distinctions on the order of milliseconds to semantic contexts which shift over seconds to minutes. It is not well understood how the brain’s speech production systems combine features at these timescales into a coherent vocal output. We investigated the spatial and temporal representations in cerebral cortex of three phonological units with different durations: consonants, vowels, and syllables. Electrocorticography (ECoG) recordings were obtained from five participants while speaking single syllables. We developed a novel clustering and Kalman filter-based trend analysis procedure to sort electrodes into temporal response profiles. A linear discriminant classifier was used to determine how strongly each electrode’s response encoded phonological features. We found distinct time-courses of encoding phonological units depending on their duration: consonants were represented more during speech preparation, vowels were represented evenly throughout trials, and syllables during production. Locations of strongly speech-encoding electrodes (the top 30% of electrodes) likewise depended on phonological element duration, with consonant-encoding electrodes left-lateralized, vowel-encoding hemispherically balanced, and syllable-encoding right-lateralized. The lateralization of speech-encoding electrodes depended on onset time, with electrodes active before or after speech production favoring left hemisphere and those active during speech favoring the right. Single-electrode speech classification revealed cortical areas with preferential encoding of particular phonemic elements, including consonant encoding in the left precentral and postcentral gyri and syllable encoding in the right middle frontal gyrus. Our findings support neurolinguistic theories of left hemisphere specialization for processing short-timescale linguistic units and right hemisphere processing of longer-duration units. Society for Neuroscience 2023-10-05 /pmc/articles/PMC10561542/ /pubmed/37739786 http://dx.doi.org/10.1523/ENEURO.0474-22.2023 Text en Copyright © 2023 Meier 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
Meier, Andrew
Kuzdeba, Scott
Jackson, Liam
Daliri, Ayoub
Tourville, Jason A.
Guenther, Frank H.
Greenlee, Jeremy D. W.
Lateralization and Time-Course of Cortical Phonological Representations during Syllable Production
title Lateralization and Time-Course of Cortical Phonological Representations during Syllable Production
title_full Lateralization and Time-Course of Cortical Phonological Representations during Syllable Production
title_fullStr Lateralization and Time-Course of Cortical Phonological Representations during Syllable Production
title_full_unstemmed Lateralization and Time-Course of Cortical Phonological Representations during Syllable Production
title_short Lateralization and Time-Course of Cortical Phonological Representations during Syllable Production
title_sort lateralization and time-course of cortical phonological representations during syllable production
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10561542/
https://www.ncbi.nlm.nih.gov/pubmed/37739786
http://dx.doi.org/10.1523/ENEURO.0474-22.2023
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