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Distinct interacting cortical networks for stimulus-response and repetition-suppression

Non-invasive studies consider the initial neural stimulus response (SR) and repetition suppression (RS) – the decreased response to repeated sensory stimuli – as engaging the same neurons. That is, RS is a suppression of the SR. We challenge this conjecture using electrocorticographic (ECoG) recordi...

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Autores principales: Eckert, David, Reichert, Christoph, Bien, Christian G., Heinze, Hans-Jochen, Knight, Robert T., Deouell, Leon Y., Dürschmid, Stefan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9445181/
https://www.ncbi.nlm.nih.gov/pubmed/36064744
http://dx.doi.org/10.1038/s42003-022-03861-4
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author Eckert, David
Reichert, Christoph
Bien, Christian G.
Heinze, Hans-Jochen
Knight, Robert T.
Deouell, Leon Y.
Dürschmid, Stefan
author_facet Eckert, David
Reichert, Christoph
Bien, Christian G.
Heinze, Hans-Jochen
Knight, Robert T.
Deouell, Leon Y.
Dürschmid, Stefan
author_sort Eckert, David
collection PubMed
description Non-invasive studies consider the initial neural stimulus response (SR) and repetition suppression (RS) – the decreased response to repeated sensory stimuli – as engaging the same neurons. That is, RS is a suppression of the SR. We challenge this conjecture using electrocorticographic (ECoG) recordings with high spatial resolution in ten patients listening to task-irrelevant trains of auditory stimuli. SR and RS were indexed by high-frequency activity (HFA) across temporal, parietal, and frontal cortices. HFA(SR) and HFA(RS) were temporally and spatially distinct, with HFA(RS) emerging later than HFA(SR) and showing only a limited spatial intersection with HFA(SR): most HFA(SR) sites did not demonstrate HFA(RS), and HFA(RS) was found where no HFA(SR) could be recorded. β activity was enhanced in HFA(RS) compared to HFA(SR) cortical sites. θ activity was enhanced in HFA(SR) compared to HFA(RS) sites. Furthermore, HFA(SR) sites propagated information to HFA(RS) sites via transient θ:β phase-phase coupling. In contrast to predictive coding (PC) accounts our results indicate that HFA(SR) and HFA(RS) are functionally linked but have minimal spatial overlap. HFA(SR) might enable stable and rapid perception of environmental stimuli across extended temporal intervals. In contrast HFA(RS) might support efficient generation of an internal model based on stimulus history.
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spelling pubmed-94451812022-09-07 Distinct interacting cortical networks for stimulus-response and repetition-suppression Eckert, David Reichert, Christoph Bien, Christian G. Heinze, Hans-Jochen Knight, Robert T. Deouell, Leon Y. Dürschmid, Stefan Commun Biol Article Non-invasive studies consider the initial neural stimulus response (SR) and repetition suppression (RS) – the decreased response to repeated sensory stimuli – as engaging the same neurons. That is, RS is a suppression of the SR. We challenge this conjecture using electrocorticographic (ECoG) recordings with high spatial resolution in ten patients listening to task-irrelevant trains of auditory stimuli. SR and RS were indexed by high-frequency activity (HFA) across temporal, parietal, and frontal cortices. HFA(SR) and HFA(RS) were temporally and spatially distinct, with HFA(RS) emerging later than HFA(SR) and showing only a limited spatial intersection with HFA(SR): most HFA(SR) sites did not demonstrate HFA(RS), and HFA(RS) was found where no HFA(SR) could be recorded. β activity was enhanced in HFA(RS) compared to HFA(SR) cortical sites. θ activity was enhanced in HFA(SR) compared to HFA(RS) sites. Furthermore, HFA(SR) sites propagated information to HFA(RS) sites via transient θ:β phase-phase coupling. In contrast to predictive coding (PC) accounts our results indicate that HFA(SR) and HFA(RS) are functionally linked but have minimal spatial overlap. HFA(SR) might enable stable and rapid perception of environmental stimuli across extended temporal intervals. In contrast HFA(RS) might support efficient generation of an internal model based on stimulus history. Nature Publishing Group UK 2022-09-05 /pmc/articles/PMC9445181/ /pubmed/36064744 http://dx.doi.org/10.1038/s42003-022-03861-4 Text en © The Author(s) 2022 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
Eckert, David
Reichert, Christoph
Bien, Christian G.
Heinze, Hans-Jochen
Knight, Robert T.
Deouell, Leon Y.
Dürschmid, Stefan
Distinct interacting cortical networks for stimulus-response and repetition-suppression
title Distinct interacting cortical networks for stimulus-response and repetition-suppression
title_full Distinct interacting cortical networks for stimulus-response and repetition-suppression
title_fullStr Distinct interacting cortical networks for stimulus-response and repetition-suppression
title_full_unstemmed Distinct interacting cortical networks for stimulus-response and repetition-suppression
title_short Distinct interacting cortical networks for stimulus-response and repetition-suppression
title_sort distinct interacting cortical networks for stimulus-response and repetition-suppression
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9445181/
https://www.ncbi.nlm.nih.gov/pubmed/36064744
http://dx.doi.org/10.1038/s42003-022-03861-4
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