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Anesthetic modulations dissociate neuroelectric characteristics between sensory-evoked and spontaneous activities across bilateral rat somatosensory cortical laminae

Spontaneous neural activity has been widely adopted to construct functional connectivity (FC) amongst distant brain regions. Although informative, the functional role and signaling mechanism of the resting state FC are not intuitive as those in stimulus/task-evoked activity. In order to bridge the g...

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Autores principales: Baek, Kwangyeol, Park, Chae Ri, Jang, Siwan, Shim, Woo Hyun, Kim, Young Ro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9270342/
https://www.ncbi.nlm.nih.gov/pubmed/35804171
http://dx.doi.org/10.1038/s41598-022-13759-0
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author Baek, Kwangyeol
Park, Chae Ri
Jang, Siwan
Shim, Woo Hyun
Kim, Young Ro
author_facet Baek, Kwangyeol
Park, Chae Ri
Jang, Siwan
Shim, Woo Hyun
Kim, Young Ro
author_sort Baek, Kwangyeol
collection PubMed
description Spontaneous neural activity has been widely adopted to construct functional connectivity (FC) amongst distant brain regions. Although informative, the functional role and signaling mechanism of the resting state FC are not intuitive as those in stimulus/task-evoked activity. In order to bridge the gap, we investigated anesthetic modulation of both resting-state and sensory-evoked activities. We used two well-studied GABAergic anesthetics of varying dose (isoflurane: 0.5–2.0% and α-chloralose: 30 and 60 mg/kg∙h) and recorded changes in electrophysiology using a pair of laminar electrode arrays that encompass the entire depth of the bilateral somatosensory cortices (S1fl) in rats. Specifically, the study focused to describe how varying anesthesia conditions affect the resting state activities and resultant FC between bilateral hemispheres in comparison to those obtained by evoked responses. As results, isoflurane decreased the amplitude of evoked responses in a dose-dependent manner mostly due to the habituation of repetitive responses. However, α-chloralose rather intensified the amplitude without exhibiting habituation. No such diverging trend was observed for the spontaneous activity, in which both anesthetics increased the signal power. For α-chloralose, overall FC was similar to that obtained with the lowest dose of isoflurane at 0.5% while higher doses of isoflurane displayed increased FC. Interestingly, only α-chloralose elicited relatively much greater increases in the ipsi-stimulus evoked response (i.e., in S1fl ipsilateral to the stimulated forelimb) than those associated with the contra-stimulus response, suggesting enhanced neuronal excitability. Taken together, the findings demonstrate modulation of the FC profiles by anesthesia is highly non-linear, possibly with a distinct underlying mechanism that affects either resting state or evoked activities differently. Further, the current study warrants thorough investigation of the basal neuronal states prior to the interpretation of resting state FC and evoked activities for accurate understanding of neural signal processing and circuitry.
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spelling pubmed-92703422022-07-10 Anesthetic modulations dissociate neuroelectric characteristics between sensory-evoked and spontaneous activities across bilateral rat somatosensory cortical laminae Baek, Kwangyeol Park, Chae Ri Jang, Siwan Shim, Woo Hyun Kim, Young Ro Sci Rep Article Spontaneous neural activity has been widely adopted to construct functional connectivity (FC) amongst distant brain regions. Although informative, the functional role and signaling mechanism of the resting state FC are not intuitive as those in stimulus/task-evoked activity. In order to bridge the gap, we investigated anesthetic modulation of both resting-state and sensory-evoked activities. We used two well-studied GABAergic anesthetics of varying dose (isoflurane: 0.5–2.0% and α-chloralose: 30 and 60 mg/kg∙h) and recorded changes in electrophysiology using a pair of laminar electrode arrays that encompass the entire depth of the bilateral somatosensory cortices (S1fl) in rats. Specifically, the study focused to describe how varying anesthesia conditions affect the resting state activities and resultant FC between bilateral hemispheres in comparison to those obtained by evoked responses. As results, isoflurane decreased the amplitude of evoked responses in a dose-dependent manner mostly due to the habituation of repetitive responses. However, α-chloralose rather intensified the amplitude without exhibiting habituation. No such diverging trend was observed for the spontaneous activity, in which both anesthetics increased the signal power. For α-chloralose, overall FC was similar to that obtained with the lowest dose of isoflurane at 0.5% while higher doses of isoflurane displayed increased FC. Interestingly, only α-chloralose elicited relatively much greater increases in the ipsi-stimulus evoked response (i.e., in S1fl ipsilateral to the stimulated forelimb) than those associated with the contra-stimulus response, suggesting enhanced neuronal excitability. Taken together, the findings demonstrate modulation of the FC profiles by anesthesia is highly non-linear, possibly with a distinct underlying mechanism that affects either resting state or evoked activities differently. Further, the current study warrants thorough investigation of the basal neuronal states prior to the interpretation of resting state FC and evoked activities for accurate understanding of neural signal processing and circuitry. Nature Publishing Group UK 2022-07-08 /pmc/articles/PMC9270342/ /pubmed/35804171 http://dx.doi.org/10.1038/s41598-022-13759-0 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Baek, Kwangyeol
Park, Chae Ri
Jang, Siwan
Shim, Woo Hyun
Kim, Young Ro
Anesthetic modulations dissociate neuroelectric characteristics between sensory-evoked and spontaneous activities across bilateral rat somatosensory cortical laminae
title Anesthetic modulations dissociate neuroelectric characteristics between sensory-evoked and spontaneous activities across bilateral rat somatosensory cortical laminae
title_full Anesthetic modulations dissociate neuroelectric characteristics between sensory-evoked and spontaneous activities across bilateral rat somatosensory cortical laminae
title_fullStr Anesthetic modulations dissociate neuroelectric characteristics between sensory-evoked and spontaneous activities across bilateral rat somatosensory cortical laminae
title_full_unstemmed Anesthetic modulations dissociate neuroelectric characteristics between sensory-evoked and spontaneous activities across bilateral rat somatosensory cortical laminae
title_short Anesthetic modulations dissociate neuroelectric characteristics between sensory-evoked and spontaneous activities across bilateral rat somatosensory cortical laminae
title_sort anesthetic modulations dissociate neuroelectric characteristics between sensory-evoked and spontaneous activities across bilateral rat somatosensory cortical laminae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9270342/
https://www.ncbi.nlm.nih.gov/pubmed/35804171
http://dx.doi.org/10.1038/s41598-022-13759-0
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