Electrical resistance of brain tissue during terminal ischemia
- 作者: Mingazov B.R.1, Vinokurova D.E.1, Zakharov A.V.1,2, Khazipov R.N.3
-
隶属关系:
- Kazan Federal University
- Kazan State Medical University
- INMED, Aix-Marseille University
- 期: 卷 18, 编号 4 (2023)
- 页面: 667-670
- 栏目: Conference proceedings
- ##submission.dateSubmitted##: 15.11.2023
- ##submission.dateAccepted##: 16.11.2023
- ##submission.datePublished##: 15.12.2023
- URL: https://genescells.ru/2313-1829/article/view/623406
- DOI: https://doi.org/10.17816/gc623406
- ID: 623406
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详细
Terminal ischemia is characterized by several electrophysiological processes, including hyperpolarization, spreading depolarization (tSD), and negative ultraslow potentials (NUP) [1]. tSD is knowin to induce depolarization of neuron membranes to roughly 0 mV, accompanied by the influx of positive ions into cells, which results in the displacement of extracellular fluids into neurons, leading to cell swelling. In addition to the movement of extracellular fluid, cerebrospinal fluid flows into the perivascular region of the penetrating vessels. These processes result in a reduction of extracellular space and brain edema [2], which can elevate the likelihood of patient mortality up to 80% [3]. The decrease in extracellular space may lead to an upsurge in the electrical resistance of the tissue, enabling it to function as an important indicator of the anatomical and functional state of the brain during traumatic injuries and hemorrhages [4].
Our goal was to assess the resistance of the extracellular space in the rat’s barrel cortex by measuring voltage step amplitudes caused by current injection between the V1 cortex and the tail vein of an animal. We used 16-channel probes with iridium electrode sites and glass microelectrodes containing Ag/AgCl conductors filled with NaCl solution. We used a metal Ag/AgCl electrode as a reference, implanted in the cerebellum. The experimental animals were euthanized via inhalation of isoflurane at a lethal concentration.
Isoflurane-induced respiratory arrest led to the subsequent development of a sequence of electrophysiological processes that included hyperpolarization, terminal spreading depression, and negative ultraslow potential. The NUP persisted throughout the entirety of the recording period (30–90 minutes), with a significant increase in extracellular space resistance occurring during this time. The rise in resistance began concurrently with the end of respiration. The resistance increased by 40 [23–57]% (median [25th–75th percentile], p=0.002, n=11) after 30 minutes of breath cessation, and by 46 [(–15)–64]% (p=0.109, n=8) after 60 minutes. The resistance demonstrated equivalent changes in all cerebral cortex depths. Additionally, the NUP amplitude following respiratory arrest had a correlation with the increase of voltage step amplitudes at 30 minutes (R=–0.713, p=0.014). The resistances measured using signals from both Ag/AgCl- and Ir electrodes did not vary in any of the experiments conducted (p=1, n=5).
Thus, the rise in electrical resistance in brain tissue was shown to initiate at the point of respiratory arrest in the animal and progresses alongside the terminal processes in the cerebral cortex. This correlation is specifically linked to the fluctuations in the negative ultraslow potential. In tDS and NUP, a significant increase in tissue edema occurs due to the movement of water from the extracellular spaces into the cells, which leads to a decrease in extracellular space volume and an increase in resistance. The process can last for several minutes and is characterized by a continuous increase in voltage step amplitudes. These results suggest that tissue resistance increases during focal ischemia, as SD and NUP are also present during the formation of the ischemic focus [5].
全文:
Terminal ischemia is characterized by several electrophysiological processes, including hyperpolarization, spreading depolarization (tSD), and negative ultraslow potentials (NUP) [1]. tSD is knowin to induce depolarization of neuron membranes to roughly 0 mV, accompanied by the influx of positive ions into cells, which results in the displacement of extracellular fluids into neurons, leading to cell swelling. In addition to the movement of extracellular fluid, cerebrospinal fluid flows into the perivascular region of the penetrating vessels. These processes result in a reduction of extracellular space and brain edema [2], which can elevate the likelihood of patient mortality up to 80% [3]. The decrease in extracellular space may lead to an upsurge in the electrical resistance of the tissue, enabling it to function as an important indicator of the anatomical and functional state of the brain during traumatic injuries and hemorrhages [4].
Our goal was to assess the resistance of the extracellular space in the rat’s barrel cortex by measuring voltage step amplitudes caused by current injection between the V1 cortex and the tail vein of an animal. We used 16-channel probes with iridium electrode sites and glass microelectrodes containing Ag/AgCl conductors filled with NaCl solution. We used a metal Ag/AgCl electrode as a reference, implanted in the cerebellum. The experimental animals were euthanized via inhalation of isoflurane at a lethal concentration.
Isoflurane-induced respiratory arrest led to the subsequent development of a sequence of electrophysiological processes that included hyperpolarization, terminal spreading depression, and negative ultraslow potential. The NUP persisted throughout the entirety of the recording period (30–90 minutes), with a significant increase in extracellular space resistance occurring during this time. The rise in resistance began concurrently with the end of respiration. The resistance increased by 40 [23–57]% (median [25th–75th percentile], p=0.002, n=11) after 30 minutes of breath cessation, and by 46 [(–15)–64]% (p=0.109, n=8) after 60 minutes. The resistance demonstrated equivalent changes in all cerebral cortex depths. Additionally, the NUP amplitude following respiratory arrest had a correlation with the increase of voltage step amplitudes at 30 minutes (R=–0.713, p=0.014). The resistances measured using signals from both Ag/AgCl- and Ir electrodes did not vary in any of the experiments conducted (p=1, n=5).
Thus, the rise in electrical resistance in brain tissue was shown to initiate at the point of respiratory arrest in the animal and progresses alongside the terminal processes in the cerebral cortex. This correlation is specifically linked to the fluctuations in the negative ultraslow potential. In tDS and NUP, a significant increase in tissue edema occurs due to the movement of water from the extracellular spaces into the cells, which leads to a decrease in extracellular space volume and an increase in resistance. The process can last for several minutes and is characterized by a continuous increase in voltage step amplitudes. These results suggest that tissue resistance increases during focal ischemia, as SD and NUP are also present during the formation of the ischemic focus [5].
作者简介
B. Mingazov
Kazan Federal University
Email: AnVZaharov@kpfu.ru
俄罗斯联邦, Kazan
D. Vinokurova
Kazan Federal University
Email: AnVZaharov@kpfu.ru
俄罗斯联邦, Kazan
A. Zakharov
Kazan Federal University; Kazan State Medical University
编辑信件的主要联系方式.
Email: AnVZaharov@kpfu.ru
俄罗斯联邦, Kazan; Kazan
R. Khazipov
INMED, Aix-Marseille University
Email: AnVZaharov@kpfu.ru
法国, Marseille
参考
- Carlson AP, Shuttleworth CW, Major S, et al. Terminal spreading depolarizations causing electrocortical silencing prior to clinical brain death: case report. Journal of Neurosurgery. 2018;131(6):1773–1779. doi: 10.3171/2018.7.JNS181478
- Juzekaeva E, Gainutdinov A, Mukhtarov M., Khazipov R. Reappraisal of anoxic spreading depolarization as a terminal event during oxygen–glucose deprivation in brain slices in vitro. Scientific Reports. 2020;10(1):18970. doi: 10.1038/s41598-020-75975-w
- Stokum JA, Gerzanich V, Simard JM. Molecular pathophysiology of cerebral edema. Journal of Cerebral Blood Flow & Metabolism. 2016;36(3):513–538. doi: 10.1177/0271678X15617172
- Makarova J, Gomez-Galan M, Herreras O. Variations in tissue resistivity and in the extension of activated neuron domains shape the voltage signal during spreading depression in the CA1 in vivo. European Journal of Neuroscience. 2008;27(2):444–456. doi: 10.1111/j.1460-9568.2008.06022.x
- Vinokurova D, Zakharov A, Chernova K, et al. Depth-profile of impairments in endothelin-1 — induced focal cortical ischemia. Journal of Cerebral Blood Flow & Metabolism. 2022;42(10):1944–1960. doi: 10.1177/0271678X221107422
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