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Neonatal Isoflurane Does Not Affect Sleep Architecture and Minimally Alters Neuronal Beta Oscillations in Adolescent Rats

General anesthetics are neurotoxic to the developing rodent and primate brains leading to neurocognitive and socio-affective impairment later in life. In addition, sleep patterns are important predictors of cognitive outcomes. Yet, little is known about how anesthetics affect sleep-wake behaviors an...

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Autores principales: Manzella, Francesca M., Gulvezan, Bethany F., Maksimovic, Stefan, Useinovic, Nemanja, Raol, Yogendra H., Joksimovic, Srdjan M., Jevtovic-Todorovic, Vesna, Todorovic, Slobodan M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8591236/
https://www.ncbi.nlm.nih.gov/pubmed/34790103
http://dx.doi.org/10.3389/fnbeh.2021.703859
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author Manzella, Francesca M.
Gulvezan, Bethany F.
Maksimovic, Stefan
Useinovic, Nemanja
Raol, Yogendra H.
Joksimovic, Srdjan M.
Jevtovic-Todorovic, Vesna
Todorovic, Slobodan M.
author_facet Manzella, Francesca M.
Gulvezan, Bethany F.
Maksimovic, Stefan
Useinovic, Nemanja
Raol, Yogendra H.
Joksimovic, Srdjan M.
Jevtovic-Todorovic, Vesna
Todorovic, Slobodan M.
author_sort Manzella, Francesca M.
collection PubMed
description General anesthetics are neurotoxic to the developing rodent and primate brains leading to neurocognitive and socio-affective impairment later in life. In addition, sleep patterns are important predictors of cognitive outcomes. Yet, little is known about how anesthetics affect sleep-wake behaviors and their corresponding oscillations. Here we examine how neonatal general anesthesia affects sleep and wake behavior and associated neuronal oscillations. We exposed male and female rat pups to either 6 h of continuous isoflurane or sham anesthesia (compressed air) at the peak of their brain development (postnatal day 7). One cohort of animals was used to examine neurotoxic insult 2 h post-anesthesia exposure. At weaning age, a second cohort of rats was implanted with cortical electroencephalogram electrodes and allowed to recover. During adolescence, we measured sleep architecture (divided into wake, non-rapid eye movement, and rapid eye movement sleep) and electroencephalogram power spectra over a 24 h period. We found that exposure to neonatal isoflurane caused extensive neurotoxicity but did not disrupt sleep architecture in adolescent rats. However, these animals had a small but significant reduction in beta oscillations, specifically in the 12–20 Hz beta 1 range, associated with wake behavior. Furthermore, beta oscillations play a critical role in cortical development, cognitive processing, and homeostatic sleep drive. We speculate that dysregulation of beta oscillations may be implicated in cognitive and socio-affective outcomes associated with neonatal anesthesia.
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spelling pubmed-85912362021-11-16 Neonatal Isoflurane Does Not Affect Sleep Architecture and Minimally Alters Neuronal Beta Oscillations in Adolescent Rats Manzella, Francesca M. Gulvezan, Bethany F. Maksimovic, Stefan Useinovic, Nemanja Raol, Yogendra H. Joksimovic, Srdjan M. Jevtovic-Todorovic, Vesna Todorovic, Slobodan M. Front Behav Neurosci Behavioral Neuroscience General anesthetics are neurotoxic to the developing rodent and primate brains leading to neurocognitive and socio-affective impairment later in life. In addition, sleep patterns are important predictors of cognitive outcomes. Yet, little is known about how anesthetics affect sleep-wake behaviors and their corresponding oscillations. Here we examine how neonatal general anesthesia affects sleep and wake behavior and associated neuronal oscillations. We exposed male and female rat pups to either 6 h of continuous isoflurane or sham anesthesia (compressed air) at the peak of their brain development (postnatal day 7). One cohort of animals was used to examine neurotoxic insult 2 h post-anesthesia exposure. At weaning age, a second cohort of rats was implanted with cortical electroencephalogram electrodes and allowed to recover. During adolescence, we measured sleep architecture (divided into wake, non-rapid eye movement, and rapid eye movement sleep) and electroencephalogram power spectra over a 24 h period. We found that exposure to neonatal isoflurane caused extensive neurotoxicity but did not disrupt sleep architecture in adolescent rats. However, these animals had a small but significant reduction in beta oscillations, specifically in the 12–20 Hz beta 1 range, associated with wake behavior. Furthermore, beta oscillations play a critical role in cortical development, cognitive processing, and homeostatic sleep drive. We speculate that dysregulation of beta oscillations may be implicated in cognitive and socio-affective outcomes associated with neonatal anesthesia. Frontiers Media S.A. 2021-11-01 /pmc/articles/PMC8591236/ /pubmed/34790103 http://dx.doi.org/10.3389/fnbeh.2021.703859 Text en Copyright © 2021 Manzella, Gulvezan, Maksimovic, Useinovic, Raol, Joksimovic, Jevtovic-Todorovic and Todorovic. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Behavioral Neuroscience
Manzella, Francesca M.
Gulvezan, Bethany F.
Maksimovic, Stefan
Useinovic, Nemanja
Raol, Yogendra H.
Joksimovic, Srdjan M.
Jevtovic-Todorovic, Vesna
Todorovic, Slobodan M.
Neonatal Isoflurane Does Not Affect Sleep Architecture and Minimally Alters Neuronal Beta Oscillations in Adolescent Rats
title Neonatal Isoflurane Does Not Affect Sleep Architecture and Minimally Alters Neuronal Beta Oscillations in Adolescent Rats
title_full Neonatal Isoflurane Does Not Affect Sleep Architecture and Minimally Alters Neuronal Beta Oscillations in Adolescent Rats
title_fullStr Neonatal Isoflurane Does Not Affect Sleep Architecture and Minimally Alters Neuronal Beta Oscillations in Adolescent Rats
title_full_unstemmed Neonatal Isoflurane Does Not Affect Sleep Architecture and Minimally Alters Neuronal Beta Oscillations in Adolescent Rats
title_short Neonatal Isoflurane Does Not Affect Sleep Architecture and Minimally Alters Neuronal Beta Oscillations in Adolescent Rats
title_sort neonatal isoflurane does not affect sleep architecture and minimally alters neuronal beta oscillations in adolescent rats
topic Behavioral Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8591236/
https://www.ncbi.nlm.nih.gov/pubmed/34790103
http://dx.doi.org/10.3389/fnbeh.2021.703859
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