Changes of neuronal activity in areas CA1 and CA3 during anoxia and normoxic or hyperoxic reoxygenation in juvenile rat organotypic hippocampal slice cultures

Hoffmann, Ulrich; Pomper, Jörn K.; Graulich, Johannes; Zeller, Melanie; Schuchmann, Sebastian; Gabriel, Siegrun; Maier, Rolf F.; Heinemann, Uwe

doi:10.1016/j.brainres.2005.11.025

Cited by 8 publications

(7 citation statements)

References 56 publications

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“…9A). As discussed below, this inhibitory effect of 0.60 ATA on the oPS response is identical to that reported for nominal hypoxia using 95% N 2 ϩ 5% CO 2 (17,18,42,44,57,76). The strong inhibitory effect of an intermediate level of oxygenation (0.60 ATA O 2 ) might be interpreted to mean that any level of Pm O 2 Ͻ0.95 ATA induces tissue slice "hypoxia," resulting in a loss of general mechanisms of neuronal excitability (33,87).…”

Section: Excitability During O 2 Manipulationsupporting

confidence: 69%

“…Consequently, the only way to study the effects of further hyperoxia (Ͼ0.95 ATA O 2 ) 1 in the brain slice preparation is to use hyperbaric pressure to produce HBO (25,50,65,66). In addition, the effects of relative hyperoxia on Pt O 2 and excitability can be studied at normobaric pressure (PB Х 1 ATA) during reoxygenation following acute exposure to an intermediate level of O 2 (0.6 ATA) or anoxia (0.0 ATA), as in previous studies (17,18,42,44), which we have termed "normobaric reoxygenation" (NBO reox ).…”

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confidence: 99%

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Hyperbaric hyperoxia and normobaric reoxygenation increase excitability and activate oxygen-induced potentiation in CA1 hippocampal neurons

Garcia¹,

Putnam

Dean

2010

Journal of Applied Physiology

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Breathing hyperbaric oxygen (HBO) is common practice in hyperbaric and diving medicine. The benefits of breathing HBO, however, are limited by the risk of central nervous system O2 toxicity, which presents as seizures. We tested the hypothesis that excitability increases in CA1 neurons of the rat hippocampal slice (400 microm) over a continuum of hyperoxia that spans normobaric and hyperbaric pressures. Amplitude changes of the orthodromic population spike were used to assess neuronal O2 sensitivity before, during, and following exposure to 0, 0.6, 0.95 (control), 2.84, and 4.54 atmospheres absolute (ATA) O2. Polarographic O2 electrodes were used to measure tissue slice PO2 (PtO2). In 0.95 ATA O2, core PtO2 at 200 microm deep was 115±16 Torr (mean±SE). Increasing O2 to 2.84 and 4.54 ATA increased core PtO2 to 1,222±77 and 2,037±157 Torr, respectively. HBO increased the orthodromic population spike amplitude and usually induced hyperexcitability (i.e., secondary population spikes) and, in addition, a long-lasting potentiation of the orthodromic population spike that we have termed "oxygen-induced potentiation" (OxIP). Exposure to 0.60 ATA O2 and hypoxia (0.00 ATA) decreased core PtO2 to 84±6 and 20±4 Torr, respectively, and abolished the orthodromic response. Reoxygenation from 0.0 or 0.6 ATA O2, however, usually produced a response similar to that of HBO: hyperexcitability and activation of OxIP. We conclude that CA1 neurons exhibit increased excitability and neural plasticity over a broad range of PtO2, which can be activated by a single, hyperoxic stimulus. We postulate that transient acute hyperoxia stimulus, whether caused by breathing HBO or reoxygenation following hypoxia (e.g., disordered breathing), is a powerful stimulant for orthodromic activity and neural plasticity in the CA1 hippocampus.

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Section: Excitability During O 2 Manipulationsupporting

confidence: 69%

mentioning

confidence: 99%

Hyperbaric hyperoxia and normobaric reoxygenation increase excitability and activate oxygen-induced potentiation in CA1 hippocampal neurons

Garcia¹,

Putnam

Dean

2010

Journal of Applied Physiology

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“…Although only a handful of brain slice studies have shown that neuronal activity is affected throughout a broad range of O 2 tensions outside of hypoxia (0% O 2 ) and the conventional control condition (95% O 2 ), these studies have shown that graded changes in O 2 , and not only hypoxia, can influence biochemical activity (D'Agostino 2007;Fowler 1993) and excitability of neurons within local networks (Fowler 1993;Garcia 3rd et al 2010;Hoffmann et al 2006;Mulkey et al 2001). Similarly, in invertebrate systems, small changes in oxygenation also have been shown to influence network activity (Clemens et al 2001).…”

Section: In Vitro Tissue Oxygenationmentioning

confidence: 99%

Graded Reductions in Oxygenation Evoke Graded Reconfiguration of the Isolated Respiratory Network

Hill

Garcia²,

Zanella

et al. 2011

Journal of Neurophysiology

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Hill AA, Garcia AJ 3rd, Zanella S, Upadhyaya R, Ramirez JM. Graded reductions in oxygenation evoke graded reconfiguration of the isolated respiratory network. J Neurophysiol 105: 625-639, 2011. First published November 17, 2010 doi:10.1152/jn.00237.2010. Neurons depend on aerobic metabolism, yet are very sensitive to oxidative stress and, as a consequence, typically operate in a low O 2 environment. The balance between blood flow and metabolic activity, both of which can vary spatially and dynamically, suggests that local O 2 availability markedly influences network output. Yet the understanding of the underlying O 2 -sensing mechanisms is limited. Are network responses regulated by discrete O 2 -sensing mechanisms or, rather, are they the consequence of inherent O 2 sensitivities of mechanisms that generate the network activity? We hypothesized that a broad range of O 2 tensions progressively modulates network activity of the preBötzinger complex (preBötC), a neuronal network critical to the central control of breathing. Rhythmogenesis was measured from the preBötC in transverse neonatal mouse brain stem slices that were exposed to graded reductions in O 2 between 0 and 95% O 2 , producing tissue oxygenation values ranging from 20 Ϯ 18 (mean Ϯ SE) to 440 Ϯ 56 Torr at the slice surface, respectively. The response of the preBötC to graded changes in O 2 is progressive for some metrics and abrupt for others, suggesting that different aspects of the respiratory network have different sensitivities to O 2 .

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“…Obstructive sleep apnea (OSA) is a multi-factorial disease involving recurrent processes of oxygen deprivation (hypoxia), hypercapnia, increased cellular production of reactive oxygen species (oxidative stress-related injury to neurons), increased cardiovascular (sympathetic) as well as ventilatory responses (for reviews, see Beebe and Gozal, 2002;Lavie, 2003;Narkiewicz and Somers, 2003;O'Driscoll and Morrell, 2005;Dincer and O'Neill, 2006). Numerous studies have utilized in vitro slice and cell culture preparations to address the cellular effects of hypoxia by exposing neurons to extremely low to 0% oxygen for prolonged periods equal to or greater than 30 minutes (Fernandez-Lopez et al, 2005;Hoffmann et al, 2006), making it difficult to correlate the resultant data with clinical findings in sleep apnea patients. An in vivo rodent model of intermittent hypoxia described by Gozal and coworkers (Gozal et al, 2001) provides correlative behavioral and anatomical consequences due to chronic intermittent hypoxia.…”

Section: In Vivo Guinea Pig Model Of Apneamentioning

confidence: 99%

Apnea promotes glutamate-induced excitotoxicity in hippocampal neurons

Fung¹,

Xi²,

Zhang³

et al. 2007

Brain Research

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Patients with obstructive sleep apnea (OSA) exhibit hippocampal damage and cognitive deficits. To determine the effect of apnea on the synaptic transmission in the hippocampus, we performed electrophysiological studies in an in vivo guinea pig model of OSA. Specifically, we determined the cornu ammonis region 1 (CA1) field excitatory postsynaptic potential (fEPSP) response to cornu ammonis region 3 (CA3) stimulation and examined the presynaptic mechanisms underlying the changes in the fEPSP. Single episodes of apnea resulted in a maximal potentiation of the fEPSPs at 1 to 3 min after the termination of each episode of apnea. The mean amplitude and slope of the post-apneic fEPSP was significantly larger compared with the pre-apneic control. These changes were accompanied by a significant decrease in the paired-pulse facilitation ratio during the post-apneic period compared with the pre-apneic control. The N-methyl-D-aspartate (NMDA) glutamate receptor antagonist MK-801, when applied locally to the CA1 recording site by pressure ejection, blocked the apnea-induced potentiation of the fEPSP. In the experimental animals that were subjected to extended periods of recurrent apnea, CA1 neurons exhibited positive immunoreactivity for fragmented DNA strands, which indicates apoptotic cell death. The present results demonstrate that apnea-induced potentiation of the hippocampal CA1 fEPSP is mediated by an NMDA receptor mechanism. We therefore conclude that recurrent apnea produces abnormally high levels of glutamate that results in the apoptosis of CA1 neurons. We hypothesize that this damage is reflected by the cognitive deficits that are commonly observed in patients with breathing disorders such as OSA.

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Changes of neuronal activity in areas CA1 and CA3 during anoxia and normoxic or hyperoxic reoxygenation in juvenile rat organotypic hippocampal slice cultures

Cited by 8 publications

References 56 publications

Hyperbaric hyperoxia and normobaric reoxygenation increase excitability and activate oxygen-induced potentiation in CA1 hippocampal neurons

Hyperbaric hyperoxia and normobaric reoxygenation increase excitability and activate oxygen-induced potentiation in CA1 hippocampal neurons

Graded Reductions in Oxygenation Evoke Graded Reconfiguration of the Isolated Respiratory Network

Apnea promotes glutamate-induced excitotoxicity in hippocampal neurons

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