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Peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally

Slow waves (SWs) are globally propagating, low-frequency (0.5- to 4-Hz) oscillations that are prominent during sleep and anesthesia. SWs are essential to neural plasticity and memory. However, much remains unknown about the mechanisms coordinating SW propagation at the macroscale. To assess SWs in t...

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Autores principales: Rosenthal, Zachary P., Raut, Ryan V., Bowen, Ryan M., Snyder, Abraham Z., Culver, Joseph P., Raichle, Marcus E., Lee, Jin-Moo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7923673/
https://www.ncbi.nlm.nih.gov/pubmed/33597303
http://dx.doi.org/10.1073/pnas.2021252118
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author Rosenthal, Zachary P.
Raut, Ryan V.
Bowen, Ryan M.
Snyder, Abraham Z.
Culver, Joseph P.
Raichle, Marcus E.
Lee, Jin-Moo
author_facet Rosenthal, Zachary P.
Raut, Ryan V.
Bowen, Ryan M.
Snyder, Abraham Z.
Culver, Joseph P.
Raichle, Marcus E.
Lee, Jin-Moo
author_sort Rosenthal, Zachary P.
collection PubMed
description Slow waves (SWs) are globally propagating, low-frequency (0.5- to 4-Hz) oscillations that are prominent during sleep and anesthesia. SWs are essential to neural plasticity and memory. However, much remains unknown about the mechanisms coordinating SW propagation at the macroscale. To assess SWs in the context of macroscale networks, we recorded cortical activity in awake and ketamine/xylazine-anesthetized mice using widefield optical imaging with fluorescent calcium indicator GCaMP6f. We demonstrate that unilateral somatosensory stimulation evokes bilateral waves that travel across the cortex with state-dependent trajectories. Under anesthesia, we observe that rhythmic stimuli elicit globally resonant, front-to-back propagating SWs. Finally, photothrombotic lesions of S1 show that somatosensory-evoked global SWs depend on bilateral recruitment of homotopic primary somatosensory cortices. Specifically, unilateral lesions of S1 disrupt somatosensory-evoked global SW initiation from either hemisphere, while spontaneous SWs are largely unchanged. These results show that evoked SWs may be triggered by bilateral activation of specific, homotopically connected cortical networks.
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spelling pubmed-79236732021-03-10 Peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally Rosenthal, Zachary P. Raut, Ryan V. Bowen, Ryan M. Snyder, Abraham Z. Culver, Joseph P. Raichle, Marcus E. Lee, Jin-Moo Proc Natl Acad Sci U S A Biological Sciences Slow waves (SWs) are globally propagating, low-frequency (0.5- to 4-Hz) oscillations that are prominent during sleep and anesthesia. SWs are essential to neural plasticity and memory. However, much remains unknown about the mechanisms coordinating SW propagation at the macroscale. To assess SWs in the context of macroscale networks, we recorded cortical activity in awake and ketamine/xylazine-anesthetized mice using widefield optical imaging with fluorescent calcium indicator GCaMP6f. We demonstrate that unilateral somatosensory stimulation evokes bilateral waves that travel across the cortex with state-dependent trajectories. Under anesthesia, we observe that rhythmic stimuli elicit globally resonant, front-to-back propagating SWs. Finally, photothrombotic lesions of S1 show that somatosensory-evoked global SWs depend on bilateral recruitment of homotopic primary somatosensory cortices. Specifically, unilateral lesions of S1 disrupt somatosensory-evoked global SW initiation from either hemisphere, while spontaneous SWs are largely unchanged. These results show that evoked SWs may be triggered by bilateral activation of specific, homotopically connected cortical networks. National Academy of Sciences 2021-02-23 2021-02-17 /pmc/articles/PMC7923673/ /pubmed/33597303 http://dx.doi.org/10.1073/pnas.2021252118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ 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
Rosenthal, Zachary P.
Raut, Ryan V.
Bowen, Ryan M.
Snyder, Abraham Z.
Culver, Joseph P.
Raichle, Marcus E.
Lee, Jin-Moo
Peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally
title Peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally
title_full Peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally
title_fullStr Peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally
title_full_unstemmed Peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally
title_short Peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally
title_sort peripheral sensory stimulation elicits global slow waves by recruiting somatosensory cortex bilaterally
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7923673/
https://www.ncbi.nlm.nih.gov/pubmed/33597303
http://dx.doi.org/10.1073/pnas.2021252118
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