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Low-dimensional neuronal population dynamics in anterior superior temporal gyrus reactivate phonetic representations during semantic processing

Traditional models of speech perception posit that neural activity sequentially encodes speech through a hierarchy of cognitive processes, from early representations of acoustic and phonetic features to late semantic encoding. Yet the mechanisms by which neural representations are transformed across...

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Autores principales: Orepic, Pavo, Truccolo, Wilson, Cash, Sydney S., Giraud, Anne-Lise, Proix, Timothée
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10634964/
https://www.ncbi.nlm.nih.gov/pubmed/37961305
http://dx.doi.org/10.1101/2023.10.30.564638
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author Orepic, Pavo
Truccolo, Wilson
Cash, Sydney S.
Giraud, Anne-Lise
Proix, Timothée
author_facet Orepic, Pavo
Truccolo, Wilson
Cash, Sydney S.
Giraud, Anne-Lise
Proix, Timothée
author_sort Orepic, Pavo
collection PubMed
description Traditional models of speech perception posit that neural activity sequentially encodes speech through a hierarchy of cognitive processes, from early representations of acoustic and phonetic features to late semantic encoding. Yet the mechanisms by which neural representations are transformed across the speech hierarchy remain poorly specified. Here, we analyzed unique microelectrode array recordings of neuronal spiking activity from the human left anterior superior temporal gyrus, a brain region at the interface between phonetic and semantic auditory processing, during a semantic categorization task and natural speech perception. In both conditions, low-dimensional neuronal population dynamics revealed a distributed and parallel encoding of phonetic and semantic representations. During natural speech, the low-dimensional dynamics were simultaneous to a power increase in the beta and low-gamma local field potentials, reflecting concurrent instantiation of top-down predictive and bottom-up cumulative processes. Our results support a mechanism for phonetic-to-semantic transformations encoded at the neuronal population level.
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spelling pubmed-106349642023-11-13 Low-dimensional neuronal population dynamics in anterior superior temporal gyrus reactivate phonetic representations during semantic processing Orepic, Pavo Truccolo, Wilson Cash, Sydney S. Giraud, Anne-Lise Proix, Timothée bioRxiv Article Traditional models of speech perception posit that neural activity sequentially encodes speech through a hierarchy of cognitive processes, from early representations of acoustic and phonetic features to late semantic encoding. Yet the mechanisms by which neural representations are transformed across the speech hierarchy remain poorly specified. Here, we analyzed unique microelectrode array recordings of neuronal spiking activity from the human left anterior superior temporal gyrus, a brain region at the interface between phonetic and semantic auditory processing, during a semantic categorization task and natural speech perception. In both conditions, low-dimensional neuronal population dynamics revealed a distributed and parallel encoding of phonetic and semantic representations. During natural speech, the low-dimensional dynamics were simultaneous to a power increase in the beta and low-gamma local field potentials, reflecting concurrent instantiation of top-down predictive and bottom-up cumulative processes. Our results support a mechanism for phonetic-to-semantic transformations encoded at the neuronal population level. Cold Spring Harbor Laboratory 2023-10-31 /pmc/articles/PMC10634964/ /pubmed/37961305 http://dx.doi.org/10.1101/2023.10.30.564638 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Orepic, Pavo
Truccolo, Wilson
Cash, Sydney S.
Giraud, Anne-Lise
Proix, Timothée
Low-dimensional neuronal population dynamics in anterior superior temporal gyrus reactivate phonetic representations during semantic processing
title Low-dimensional neuronal population dynamics in anterior superior temporal gyrus reactivate phonetic representations during semantic processing
title_full Low-dimensional neuronal population dynamics in anterior superior temporal gyrus reactivate phonetic representations during semantic processing
title_fullStr Low-dimensional neuronal population dynamics in anterior superior temporal gyrus reactivate phonetic representations during semantic processing
title_full_unstemmed Low-dimensional neuronal population dynamics in anterior superior temporal gyrus reactivate phonetic representations during semantic processing
title_short Low-dimensional neuronal population dynamics in anterior superior temporal gyrus reactivate phonetic representations during semantic processing
title_sort low-dimensional neuronal population dynamics in anterior superior temporal gyrus reactivate phonetic representations during semantic processing
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10634964/
https://www.ncbi.nlm.nih.gov/pubmed/37961305
http://dx.doi.org/10.1101/2023.10.30.564638
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