Ion channel involvement in hypoxia-induced spreading depression in hippocampal slices

Aitken, Peter G.; Jing, Jian; Young, Jacob N.; Somjen, George G.

doi:10.1016/0006-8993(91)91067-b

Cited by 64 publications

(37 citation statements)

References 31 publications

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“…6, red trace). Our result is consistent with previous findings that seizures are related to mild hypoxia, while spreading depression is related to more severe hypoxia (Aitken et al 1991;Bahar et al 2000) and the mixture state of seizure and spreading depression seen in hypoxia (Czéh et al 1993). The pattern from the red trace is also seen experimentally in OLM cells and occasionally pyramidal cells during seizures when they go into transient depolarization block (Žiburkus et al 2006, 2013 Fig.…”

Section: (Companion Article)supporting

confidence: 92%

Oxygen and seizure dynamics: II. Computational modeling

Wei

Ullah

Ingram

et al. 2014

Journal of Neurophysiology

126

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recordings show intense neuronal firing during epileptic seizures leading to enhanced energy consumption. However, the relationship between oxygen metabolism and seizure patterns has not been well studied. Recent studies have developed fast and quantitative techniques to measure oxygen microdomain concentration during seizure events. In this article, we develop a biophysical model that accounts for these experimental observations. The model is an extension of the Hodgkin-Huxley formalism and includes the neuronal microenvironment dynamics of sodium, potassium, and oxygen concentrations. Our model accounts for metabolic energy consumption during and following seizure events. We can further account for the experimental observation that hypoxia can induce seizures, with seizures occurring only within a narrow range of tissue oxygen pressure. We also reproduce the interplay between excitatory and inhibitory neurons seen in experiments, accounting for the different oxygen levels observed during seizures in excitatory vs. inhibitory cell layers. Our findings offer a more comprehensive understanding of the complex interrelationship among seizures, ion dynamics, and energy metabolism.hippocampus; hypoxia; bifurcation; epilepsy; potassium THE BRAIN CONSUMES 20% OF the body's metabolic energy with muscles and digestive system at rest, despite being only 2% of the human body mass (Attwell and Laughlin 2001). The majority of the brain's metabolic energy is dedicated to supporting neural spiking activity, most of which is used by Na ϩ -K ϩ

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Section: (Companion Article)supporting

confidence: 92%

Oxygen and seizure dynamics: II. Computational modeling

Wei

Ullah

Ingram

et al. 2014

Journal of Neurophysiology

126

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“…In vitro experiments show that the delay cannot be attributed to the dead volume of the microdialysis system. In addition, spreading depression is not mediated by voltage-gated sodium IFr by r~iLX\ channels (Tobiasz & Nicholson 1982;Aitken et al, 1991), but in the present study, tetrodotoxin significantly reduced the effect of topically applied drugs. Furthermore a previous study using this paradigm showed that infusion of drugs into the 3 6 9 --frontal cortex had a similar effect to topical application of the 3 6 9 12 15 drugs to the same frontal region (Palmer et al, 1989).…”

Section: Discussionmentioning

confidence: 44%

NMDA‐induced glutamate and aspartate release from rat cortical pyramidal neurones: evidence for modulation by a 5‐HT_1A antagonist

Dijk¹,

Francis²,

Stratmann³

et al. 1995

British J Pharmacology

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1 We have investigated an aspect of the regulation of cortical pyramidal neurone activity. Microdialysis was used to assess whether topical application of drugs (in 10 M1) to fill a burr hole over the frontal cortex, where part of the corticostriatal pathway originates, would change concentrations of the excitatory amino acids glutamate and aspartate in the striatum of the anaesthetized rat. 2 Topical application of N-methyl-D-aspartate (NMDA, 2 and 20 mM) dose-dependently increased glutamate and aspartate concentrations in the striatum. Coapplication of tetrodotoxin (10 ,uM) blocked the NMDA-evoked rise in these amino acids. A calcium-free medium, perfused through the probe also blocked the rise, indicating that it was due to an exocytotic mechanism in the striatum. 3 It was hypothesized that the rise observed was due to an increase in the activity of the corticostriatal pathway. As 5-hydroxytryptaminelA (5-HTIA) receptors are enriched on cell bodies of corticostriatal neurones, a selective 5-HTIA-antagonist (WAY 100135)

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“…Experiments on voluntary apneas have shown acute and lasting effects on autonomic regulation of the cardiovascular system and increased sympathetic nerve activity caused by hypoxia [81,82]. Hypoxia has also been shown to induce hypoxic spreading depression-like depolarization in areas throughout the brain, including hippocampal [83] and cortical tissues [84]. We propose that this well-documented hypoxic depolarization occurs on a much smaller scale during each expiration.…”

Section: Breath-holding and Breathing Disordersmentioning

confidence: 79%

Widespread depolarization during expiration: A source of respiratory drive?

Jerath¹,

Crawford²,

Barnes

et al. 2015

Medical Hypotheses

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a b s t r a c tRespiration influences various pacemakers and rhythms of the body during inspiration and expiration but the underlying mechanisms are relatively unknown. Understanding this phenomenon is important, as breathing disorders, breath holding, and hyperventilation can lead to significant medical conditions. We discuss the physiological modulation of heart rhythm, blood pressure, sympathetic nerve activity, EEG, and other changes observed during inspiration and expiration. We also correlate the intracellular mitochondrial respiratory metabolic processes with real-time breathing and correlate membrane potential changes with inspiration and expiration. We propose that widespread minor hyperpolarization occurs during inspiration and widespread minor depolarization occurs during expiration. This depolarization is likely a source of respiratory drive. Further knowledge of intracellular and extracellular ionic changes associated with respiration will enhance our understanding of respiration and its role as a modulator of cellular membrane potential. This could expand treatment options for a wide range of health conditions, such as breathing disorders, stress-related disorders, and further our understanding of the Hering-Breuer reflex and respiratory sinus arrhythmia.Ó 2014 Elsevier Ltd. All rights reserved. IntroductionIn addition to gas exchange and oxygenation of the blood, respiration in the lungs can regulate multiple physiological processes throughout the body. Studies of the cardiovascular system, the peripheral nervous system, and the central nervous system provide evidence that respiratory patterns can exert a significant and immediate influence on a wide range of bodily functions, including changes in blood pressure and sympathovagal balance. Patterned respiration can regulate blood pressure and heart rate [1], as well as regulate rhythmic centers of the brain that control cardiovascular output [2,3]. While the majority of these findings have demonstrated the impact of respiration on cardiac output and other processes in isolated preparations, little work has focused on respiration's direct influence on membrane potential.This article reviews the current understanding of respiration as a regulator of cardiovascular physiology and nervous system function. More specifically, we discuss the role of respiratory rhythm and rate on both systemic and local control of these systems. We describe the role of pulmonary stretch receptors (with a focus on slowly adapting receptors) in converting breathing patterns into a functional, multi-faceted, mechanism that allows respiration to communicate with, and direct various aspects of cardiovascular and nervous system physiology. We propose a hypothesis in which inspiration and expiration are associated with transient increases and decreases in membrane potential that may underlie these widespread changes and how these membrane potential changes may underlie the chaotic dynamics of rhythmic breathing.Many studies focus on the brainstem as the primary modulator of resp...

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Ion channel involvement in hypoxia-induced spreading depression in hippocampal slices

Cited by 64 publications

References 31 publications

Oxygen and seizure dynamics: II. Computational modeling

Oxygen and seizure dynamics: II. Computational modeling

NMDA‐induced glutamate and aspartate release from rat cortical pyramidal neurones: evidence for modulation by a 5‐HT_1A antagonist

Widespread depolarization during expiration: A source of respiratory drive?

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Ion channel involvement in hypoxia-induced spreading depression in hippocampal slices

Cited by 64 publications

References 31 publications

Oxygen and seizure dynamics: II. Computational modeling

Oxygen and seizure dynamics: II. Computational modeling

NMDA‐induced glutamate and aspartate release from rat cortical pyramidal neurones: evidence for modulation by a 5‐HT1A antagonist

Widespread depolarization during expiration: A source of respiratory drive?

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NMDA‐induced glutamate and aspartate release from rat cortical pyramidal neurones: evidence for modulation by a 5‐HT_1A antagonist