Anoxic spreading depolarization in the neonatal rat cortex in vitro

Anoxic spreading depolarization (aSD) is a hallmark of ischemic injury in the cerebral cortex. In adults, aSD is associated with rapid and nearly complete neuronal depolarization and loss of neuronal functions. While ischemia also evokes aSD in the immature cortex, developmental aspects of neuronal...

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Main Authors: Azat Gainutdinov, Elvira Juzekaeva, Marat Mukhtarov, Roustem Khazipov
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-03-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fncel.2023.1106268/full
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author Azat Gainutdinov
Azat Gainutdinov
Elvira Juzekaeva
Marat Mukhtarov
Roustem Khazipov
Roustem Khazipov
author_facet Azat Gainutdinov
Azat Gainutdinov
Elvira Juzekaeva
Marat Mukhtarov
Roustem Khazipov
Roustem Khazipov
author_sort Azat Gainutdinov
collection DOAJ
description Anoxic spreading depolarization (aSD) is a hallmark of ischemic injury in the cerebral cortex. In adults, aSD is associated with rapid and nearly complete neuronal depolarization and loss of neuronal functions. While ischemia also evokes aSD in the immature cortex, developmental aspects of neuronal behavior during aSD remain largely unknown. Here, using oxygen-glucose deprivation (OGD) ischemia model in slices of the postnatal rat somatosensory cortex, we found that immature neurons displayed much more complex behaviors: they initially moderately depolarized during aSD, then transiently repolarised (for up to tens of minutes), and only then passed to terminal depolarization. The ability to fire action potentials was maintained in neurons mildly depolarized during aSD without reaching the level of depolarization block, and these functions were regained in the majority of immature neurons during post-aSD transient repolarization. The amplitude of depolarization and the probability of depolarization block during aSD increased, whereas transient post-SD repolarization levels and duration, and associated recovery in neuronal firing decreased with age. By the end of the first postnatal month, aSD acquired an adult-like phenotype, where depolarization during aSD merged with terminal depolarization and the phase of transient recovery was lost. Thus, changes in neuronal function during aSD undergo remarkable developmental changes that may contribute to lower susceptibility of the immature neurons to ischemia.
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spelling doaj.art-7619037ee8cc4d42b6bd6534aa46f7892023-03-09T06:40:49ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022023-03-011710.3389/fncel.2023.11062681106268Anoxic spreading depolarization in the neonatal rat cortex in vitroAzat Gainutdinov0Azat Gainutdinov1Elvira Juzekaeva2Marat Mukhtarov3Roustem Khazipov4Roustem Khazipov5Laboratory of Neurobiology, Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, RussiaINMED—INSERM, Aix-Marseille University, Marseille, FranceLaboratory of Neurobiology, Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, RussiaLaboratory of Neurobiology, Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, RussiaLaboratory of Neurobiology, Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, RussiaINMED—INSERM, Aix-Marseille University, Marseille, FranceAnoxic spreading depolarization (aSD) is a hallmark of ischemic injury in the cerebral cortex. In adults, aSD is associated with rapid and nearly complete neuronal depolarization and loss of neuronal functions. While ischemia also evokes aSD in the immature cortex, developmental aspects of neuronal behavior during aSD remain largely unknown. Here, using oxygen-glucose deprivation (OGD) ischemia model in slices of the postnatal rat somatosensory cortex, we found that immature neurons displayed much more complex behaviors: they initially moderately depolarized during aSD, then transiently repolarised (for up to tens of minutes), and only then passed to terminal depolarization. The ability to fire action potentials was maintained in neurons mildly depolarized during aSD without reaching the level of depolarization block, and these functions were regained in the majority of immature neurons during post-aSD transient repolarization. The amplitude of depolarization and the probability of depolarization block during aSD increased, whereas transient post-SD repolarization levels and duration, and associated recovery in neuronal firing decreased with age. By the end of the first postnatal month, aSD acquired an adult-like phenotype, where depolarization during aSD merged with terminal depolarization and the phase of transient recovery was lost. Thus, changes in neuronal function during aSD undergo remarkable developmental changes that may contribute to lower susceptibility of the immature neurons to ischemia.https://www.frontiersin.org/articles/10.3389/fncel.2023.1106268/fullpatch-clampmembrane potentialischemiasomatosensory cortexspreading depolarizationneonate
spellingShingle Azat Gainutdinov
Azat Gainutdinov
Elvira Juzekaeva
Marat Mukhtarov
Roustem Khazipov
Roustem Khazipov
Anoxic spreading depolarization in the neonatal rat cortex in vitro
Frontiers in Cellular Neuroscience
patch-clamp
membrane potential
ischemia
somatosensory cortex
spreading depolarization
neonate
title Anoxic spreading depolarization in the neonatal rat cortex in vitro
title_full Anoxic spreading depolarization in the neonatal rat cortex in vitro
title_fullStr Anoxic spreading depolarization in the neonatal rat cortex in vitro
title_full_unstemmed Anoxic spreading depolarization in the neonatal rat cortex in vitro
title_short Anoxic spreading depolarization in the neonatal rat cortex in vitro
title_sort anoxic spreading depolarization in the neonatal rat cortex in vitro
topic patch-clamp
membrane potential
ischemia
somatosensory cortex
spreading depolarization
neonate
url https://www.frontiersin.org/articles/10.3389/fncel.2023.1106268/full
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