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Propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness

During propofol-induced general anesthesia, alpha rhythms measured using electroencephalography undergo a striking shift from posterior to anterior, termed anteriorization, where the ubiquitous waking alpha is lost and a frontal alpha emerges. The functional significance of alpha anteriorization and...

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Autores principales: Weiner, Veronica S., Zhou, David W., Kahali, Pegah, Stephen, Emily P., Peterfreund, Robert A., Aglio, Linda S., Szabo, Michele D., Eskandar, Emad N., Salazar-Gomez, Andrés F., Sampson, Aaron L., Cash, Sydney S., Brown, Emery N., Purdon, Patrick L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10089159/
https://www.ncbi.nlm.nih.gov/pubmed/36897972
http://dx.doi.org/10.1073/pnas.2207831120
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author Weiner, Veronica S.
Zhou, David W.
Kahali, Pegah
Stephen, Emily P.
Peterfreund, Robert A.
Aglio, Linda S.
Szabo, Michele D.
Eskandar, Emad N.
Salazar-Gomez, Andrés F.
Sampson, Aaron L.
Cash, Sydney S.
Brown, Emery N.
Purdon, Patrick L.
author_facet Weiner, Veronica S.
Zhou, David W.
Kahali, Pegah
Stephen, Emily P.
Peterfreund, Robert A.
Aglio, Linda S.
Szabo, Michele D.
Eskandar, Emad N.
Salazar-Gomez, Andrés F.
Sampson, Aaron L.
Cash, Sydney S.
Brown, Emery N.
Purdon, Patrick L.
author_sort Weiner, Veronica S.
collection PubMed
description During propofol-induced general anesthesia, alpha rhythms measured using electroencephalography undergo a striking shift from posterior to anterior, termed anteriorization, where the ubiquitous waking alpha is lost and a frontal alpha emerges. The functional significance of alpha anteriorization and the precise brain regions contributing to the phenomenon are a mystery. While posterior alpha is thought to be generated by thalamocortical circuits connecting nuclei of the sensory thalamus with their cortical partners, the thalamic origins of the propofol-induced alpha remain poorly understood. Here, we used human intracranial recordings to identify regions in sensory cortices where propofol attenuates a coherent alpha network, distinct from those in the frontal cortex where it amplifies coherent alpha and beta activities. We then performed diffusion tractography between these identified regions and individual thalamic nuclei to show that the opposing dynamics of anteriorization occur within two distinct thalamocortical networks. We found that propofol disrupted a posterior alpha network structurally connected with nuclei in the sensory and sensory associational regions of the thalamus. At the same time, propofol induced a coherent alpha oscillation within prefrontal cortical areas that were connected with thalamic nuclei involved in cognition, such as the mediodorsal nucleus. The cortical and thalamic anatomy involved, as well as their known functional roles, suggests multiple means by which propofol dismantles sensory and cognitive processes to achieve loss of consciousness.
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spelling pubmed-100891592023-04-12 Propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness Weiner, Veronica S. Zhou, David W. Kahali, Pegah Stephen, Emily P. Peterfreund, Robert A. Aglio, Linda S. Szabo, Michele D. Eskandar, Emad N. Salazar-Gomez, Andrés F. Sampson, Aaron L. Cash, Sydney S. Brown, Emery N. Purdon, Patrick L. Proc Natl Acad Sci U S A Biological Sciences During propofol-induced general anesthesia, alpha rhythms measured using electroencephalography undergo a striking shift from posterior to anterior, termed anteriorization, where the ubiquitous waking alpha is lost and a frontal alpha emerges. The functional significance of alpha anteriorization and the precise brain regions contributing to the phenomenon are a mystery. While posterior alpha is thought to be generated by thalamocortical circuits connecting nuclei of the sensory thalamus with their cortical partners, the thalamic origins of the propofol-induced alpha remain poorly understood. Here, we used human intracranial recordings to identify regions in sensory cortices where propofol attenuates a coherent alpha network, distinct from those in the frontal cortex where it amplifies coherent alpha and beta activities. We then performed diffusion tractography between these identified regions and individual thalamic nuclei to show that the opposing dynamics of anteriorization occur within two distinct thalamocortical networks. We found that propofol disrupted a posterior alpha network structurally connected with nuclei in the sensory and sensory associational regions of the thalamus. At the same time, propofol induced a coherent alpha oscillation within prefrontal cortical areas that were connected with thalamic nuclei involved in cognition, such as the mediodorsal nucleus. The cortical and thalamic anatomy involved, as well as their known functional roles, suggests multiple means by which propofol dismantles sensory and cognitive processes to achieve loss of consciousness. National Academy of Sciences 2023-03-10 2023-03-14 /pmc/articles/PMC10089159/ /pubmed/36897972 http://dx.doi.org/10.1073/pnas.2207831120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Weiner, Veronica S.
Zhou, David W.
Kahali, Pegah
Stephen, Emily P.
Peterfreund, Robert A.
Aglio, Linda S.
Szabo, Michele D.
Eskandar, Emad N.
Salazar-Gomez, Andrés F.
Sampson, Aaron L.
Cash, Sydney S.
Brown, Emery N.
Purdon, Patrick L.
Propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness
title Propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness
title_full Propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness
title_fullStr Propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness
title_full_unstemmed Propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness
title_short Propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness
title_sort propofol disrupts alpha dynamics in functionally distinct thalamocortical networks during loss of consciousness
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10089159/
https://www.ncbi.nlm.nih.gov/pubmed/36897972
http://dx.doi.org/10.1073/pnas.2207831120
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