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Spatio-Temporal Progression of Cortical Activity Related to Continuous Overt and Covert Speech Production in a Reading Task

How the human brain plans, executes, and monitors continuous and fluent speech has remained largely elusive. For example, previous research has defined the cortical locations most important for different aspects of speech function, but has not yet yielded a definition of the temporal progression of...

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Autores principales: Brumberg, Jonathan S., Krusienski, Dean J., Chakrabarti, Shreya, Gunduz, Aysegul, Brunner, Peter, Ritaccio, Anthony L., Schalk, Gerwin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5119784/
https://www.ncbi.nlm.nih.gov/pubmed/27875590
http://dx.doi.org/10.1371/journal.pone.0166872
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author Brumberg, Jonathan S.
Krusienski, Dean J.
Chakrabarti, Shreya
Gunduz, Aysegul
Brunner, Peter
Ritaccio, Anthony L.
Schalk, Gerwin
author_facet Brumberg, Jonathan S.
Krusienski, Dean J.
Chakrabarti, Shreya
Gunduz, Aysegul
Brunner, Peter
Ritaccio, Anthony L.
Schalk, Gerwin
author_sort Brumberg, Jonathan S.
collection PubMed
description How the human brain plans, executes, and monitors continuous and fluent speech has remained largely elusive. For example, previous research has defined the cortical locations most important for different aspects of speech function, but has not yet yielded a definition of the temporal progression of involvement of those locations as speech progresses either overtly or covertly. In this paper, we uncovered the spatio-temporal evolution of neuronal population-level activity related to continuous overt speech, and identified those locations that shared activity characteristics across overt and covert speech. Specifically, we asked subjects to repeat continuous sentences aloud or silently while we recorded electrical signals directly from the surface of the brain (electrocorticography (ECoG)). We then determined the relationship between cortical activity and speech output across different areas of cortex and at sub-second timescales. The results highlight a spatio-temporal progression of cortical involvement in the continuous speech process that initiates utterances in frontal-motor areas and ends with the monitoring of auditory feedback in superior temporal gyrus. Direct comparison of cortical activity related to overt versus covert conditions revealed a common network of brain regions involved in speech that may implement orthographic and phonological processing. Our results provide one of the first characterizations of the spatiotemporal electrophysiological representations of the continuous speech process, and also highlight the common neural substrate of overt and covert speech. These results thereby contribute to a refined understanding of speech functions in the human brain.
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spelling pubmed-51197842016-12-15 Spatio-Temporal Progression of Cortical Activity Related to Continuous Overt and Covert Speech Production in a Reading Task Brumberg, Jonathan S. Krusienski, Dean J. Chakrabarti, Shreya Gunduz, Aysegul Brunner, Peter Ritaccio, Anthony L. Schalk, Gerwin PLoS One Research Article How the human brain plans, executes, and monitors continuous and fluent speech has remained largely elusive. For example, previous research has defined the cortical locations most important for different aspects of speech function, but has not yet yielded a definition of the temporal progression of involvement of those locations as speech progresses either overtly or covertly. In this paper, we uncovered the spatio-temporal evolution of neuronal population-level activity related to continuous overt speech, and identified those locations that shared activity characteristics across overt and covert speech. Specifically, we asked subjects to repeat continuous sentences aloud or silently while we recorded electrical signals directly from the surface of the brain (electrocorticography (ECoG)). We then determined the relationship between cortical activity and speech output across different areas of cortex and at sub-second timescales. The results highlight a spatio-temporal progression of cortical involvement in the continuous speech process that initiates utterances in frontal-motor areas and ends with the monitoring of auditory feedback in superior temporal gyrus. Direct comparison of cortical activity related to overt versus covert conditions revealed a common network of brain regions involved in speech that may implement orthographic and phonological processing. Our results provide one of the first characterizations of the spatiotemporal electrophysiological representations of the continuous speech process, and also highlight the common neural substrate of overt and covert speech. These results thereby contribute to a refined understanding of speech functions in the human brain. Public Library of Science 2016-11-22 /pmc/articles/PMC5119784/ /pubmed/27875590 http://dx.doi.org/10.1371/journal.pone.0166872 Text en © 2016 Brumberg et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://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
Brumberg, Jonathan S.
Krusienski, Dean J.
Chakrabarti, Shreya
Gunduz, Aysegul
Brunner, Peter
Ritaccio, Anthony L.
Schalk, Gerwin
Spatio-Temporal Progression of Cortical Activity Related to Continuous Overt and Covert Speech Production in a Reading Task
title Spatio-Temporal Progression of Cortical Activity Related to Continuous Overt and Covert Speech Production in a Reading Task
title_full Spatio-Temporal Progression of Cortical Activity Related to Continuous Overt and Covert Speech Production in a Reading Task
title_fullStr Spatio-Temporal Progression of Cortical Activity Related to Continuous Overt and Covert Speech Production in a Reading Task
title_full_unstemmed Spatio-Temporal Progression of Cortical Activity Related to Continuous Overt and Covert Speech Production in a Reading Task
title_short Spatio-Temporal Progression of Cortical Activity Related to Continuous Overt and Covert Speech Production in a Reading Task
title_sort spatio-temporal progression of cortical activity related to continuous overt and covert speech production in a reading task
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5119784/
https://www.ncbi.nlm.nih.gov/pubmed/27875590
http://dx.doi.org/10.1371/journal.pone.0166872
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