Cargando…

Degeneracy in the neurological model of auditory speech repetition

Both classic and contemporary models of auditory word repetition involve at least four left hemisphere regions: primary auditory cortex for processing sounds; pSTS (within Wernicke’s area) for processing auditory images of speech; pOp (within Broca’s area) for processing motor images of speech; and...

Descripción completa

Detalles Bibliográficos
Autores principales: Sajid, Noor, Gajardo-Vidal, Andrea, Ekert, Justyna O., Lorca-Puls, Diego L., Hope, Thomas M. H., Green, David W., Friston, Karl J., Price, Cathy J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10643365/
https://www.ncbi.nlm.nih.gov/pubmed/37957231
http://dx.doi.org/10.1038/s42003-023-05515-5
_version_ 1785147098773061632
author Sajid, Noor
Gajardo-Vidal, Andrea
Ekert, Justyna O.
Lorca-Puls, Diego L.
Hope, Thomas M. H.
Green, David W.
Friston, Karl J.
Price, Cathy J.
author_facet Sajid, Noor
Gajardo-Vidal, Andrea
Ekert, Justyna O.
Lorca-Puls, Diego L.
Hope, Thomas M. H.
Green, David W.
Friston, Karl J.
Price, Cathy J.
author_sort Sajid, Noor
collection PubMed
description Both classic and contemporary models of auditory word repetition involve at least four left hemisphere regions: primary auditory cortex for processing sounds; pSTS (within Wernicke’s area) for processing auditory images of speech; pOp (within Broca’s area) for processing motor images of speech; and primary motor cortex for overt speech articulation. Previous functional-MRI (fMRI) studies confirm that auditory repetition activates these regions, in addition to many others. Crucially, however, contemporary models do not specify how regions interact and drive each other during auditory repetition. Here, we used dynamic causal modelling, to test the functional interplay among the four core brain regions during single auditory word and pseudoword repetition. Our analysis is grounded in the principle of degeneracy—i.e., many-to-one structure-function relationships—where multiple neural pathways can execute the same function. Contrary to expectation, we found that, for both word and pseudoword repetition, (i) the effective connectivity between pSTS and pOp was predominantly bidirectional and inhibitory; (ii) activity in the motor cortex could be driven by either pSTS or pOp; and (iii) the latter varied both within and between individuals. These results suggest that different neural pathways can support auditory speech repetition. This degeneracy may explain resilience to functional loss after brain damage.
format Online
Article
Text
id pubmed-10643365
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-106433652023-11-13 Degeneracy in the neurological model of auditory speech repetition Sajid, Noor Gajardo-Vidal, Andrea Ekert, Justyna O. Lorca-Puls, Diego L. Hope, Thomas M. H. Green, David W. Friston, Karl J. Price, Cathy J. Commun Biol Article Both classic and contemporary models of auditory word repetition involve at least four left hemisphere regions: primary auditory cortex for processing sounds; pSTS (within Wernicke’s area) for processing auditory images of speech; pOp (within Broca’s area) for processing motor images of speech; and primary motor cortex for overt speech articulation. Previous functional-MRI (fMRI) studies confirm that auditory repetition activates these regions, in addition to many others. Crucially, however, contemporary models do not specify how regions interact and drive each other during auditory repetition. Here, we used dynamic causal modelling, to test the functional interplay among the four core brain regions during single auditory word and pseudoword repetition. Our analysis is grounded in the principle of degeneracy—i.e., many-to-one structure-function relationships—where multiple neural pathways can execute the same function. Contrary to expectation, we found that, for both word and pseudoword repetition, (i) the effective connectivity between pSTS and pOp was predominantly bidirectional and inhibitory; (ii) activity in the motor cortex could be driven by either pSTS or pOp; and (iii) the latter varied both within and between individuals. These results suggest that different neural pathways can support auditory speech repetition. This degeneracy may explain resilience to functional loss after brain damage. Nature Publishing Group UK 2023-11-13 /pmc/articles/PMC10643365/ /pubmed/37957231 http://dx.doi.org/10.1038/s42003-023-05515-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Sajid, Noor
Gajardo-Vidal, Andrea
Ekert, Justyna O.
Lorca-Puls, Diego L.
Hope, Thomas M. H.
Green, David W.
Friston, Karl J.
Price, Cathy J.
Degeneracy in the neurological model of auditory speech repetition
title Degeneracy in the neurological model of auditory speech repetition
title_full Degeneracy in the neurological model of auditory speech repetition
title_fullStr Degeneracy in the neurological model of auditory speech repetition
title_full_unstemmed Degeneracy in the neurological model of auditory speech repetition
title_short Degeneracy in the neurological model of auditory speech repetition
title_sort degeneracy in the neurological model of auditory speech repetition
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10643365/
https://www.ncbi.nlm.nih.gov/pubmed/37957231
http://dx.doi.org/10.1038/s42003-023-05515-5
work_keys_str_mv AT sajidnoor degeneracyintheneurologicalmodelofauditoryspeechrepetition
AT gajardovidalandrea degeneracyintheneurologicalmodelofauditoryspeechrepetition
AT ekertjustynao degeneracyintheneurologicalmodelofauditoryspeechrepetition
AT lorcapulsdiegol degeneracyintheneurologicalmodelofauditoryspeechrepetition
AT hopethomasmh degeneracyintheneurologicalmodelofauditoryspeechrepetition
AT greendavidw degeneracyintheneurologicalmodelofauditoryspeechrepetition
AT fristonkarlj degeneracyintheneurologicalmodelofauditoryspeechrepetition
AT pricecathyj degeneracyintheneurologicalmodelofauditoryspeechrepetition