Effect of anoxia on excitatory amino acids in brain slices of rats and turtles: in vitro microdialysis

Young, Richard S.; During, MJ; Donnelly, David F.; Aquila, William J.; Perry, Victor L; Haddad, Gabriel G.

doi:10.1152/ajpregu.1993.264.4.r716

Cited by 11 publications

(11 citation statements)

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“…This is a time frame that coincides with current in vivo study results. Several mechanisms have been proposed to contrib ute to the developmental differences; in creases in excitatory amino acid concentra tions, adenosine triphosphate-dependent po tassium channels, and voltage-sensitive sodi Maturation of Anoxia-Induced Gasping um channels have all been shown to modulate neuronal responses to hypoxia and anoxia [28][29][30], However, such issues are clearly beyond the scope of our study.…”

Section: Discussionmentioning

confidence: 91%

Characterization and Developmental Aspects of Anoxia-Induced Gasping in the Rat

et al. 1996

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With increasing postnatal age, mammals display diminished tolerances for prolonged exposures to severe oxygen deprivation. Similarly, duration and efficiency of gasping, a unique mechanism for enhancing survival after anoxia-induced apnea, are also affected by postnatal age. We hypothesized that maturational patterns of anoxia-induced gasping may encompass more than a single monophasic phenomenon. Each of the putative phases of the gasping response may underlie unique characteristics which could be of relevance to survival capability. To study these issues, adult rats and rat pups at 2–3, 5, 10, 15, and 25 days of age underwent anoxic exposures with 100% N₂ in a barometric chamber. In pups aged < 25 days but not thereafter, following an age-dependent period of central apnea, an initial gasping phase characterized by vigorous and frequent periodic bursts of a large inspiratory effort preceded and followed by expiration excursions emerged (phase I). This phase was followed by a period of relative respiratory silence of variable duration with occasional, interspersed phase I-like gasps (phase II). Finally, a third phase easily recognized by the onset of frequent inspiratory-only gasping efforts developed (phase III). The amplitude of phase III inspiratory gasps progressively diminished until their complete cessation. Although overlap between gasping phases was present, a marked age dependency in both duration and gasping frequency within each phase occurred. We conclude that anoxia-induced gasping responses in rat pups < 25 days old are triphasic in nature, exhibit defined phase-locked periodicities and respiratory effort patterns, and undergo significant maturation.

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Section: Discussionmentioning

confidence: 91%

Characterization and Developmental Aspects of Anoxia-Induced Gasping in the Rat

et al. 1996

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“…In the turtle Trachemys scripta, alanine concentrations between 0.16·mmol·l -1 (heart and liver) and 1.08·mmol·l -1 (white muscle) decreased pyruvate kinase activity by 50% (Brooks and Storey, 1989). An increase in brain [alanine] during anoxia/ischemia appears to be a common vertebrate response, having been found in the anoxic turtle crucian carp (Hylland and Nilsson, 1999) and neonate rat as well as the ischemic adult rat brain (Erecinska et al, 1984;Young et al, 1993). It has been suggested that increasing alanine levels may even be a preferred indicator of severe hypoxia, as lactate is a reliable indicator of only mild hypoxia (Ben-Yoseph et al, 1993).…”

Section: Alaninementioning

confidence: 99%

“…The lack of extracellular increase, however, is noteworthy, as pathological increases in extracellular glutamate levels are thought to play a central role in hypoxic/ischemic neuronal degeneration and reperfusion injuries (Globus et al, 1988;Choi, 1992). Extracellular glutamate levels may increase as much as 37-fold in the ischemic rat brain (Goda et al, 1998), while Young et al (1993) found that levels in anoxic rat brain slices more than doubled in 10·min. Excess glutamate then activates ionotropic and metabotropic receptors, triggering a cascade of events resulting in neuronal death.…”

Section: Aspartate Glutamate and Glutaminementioning

confidence: 99%

“…In the turtle, extracellular glutamate and dopamine are maintained at basal levels during extended anoxia Milton and Lutz, 1998), while levels of inhibitory neuroactive compounds such as GABA and glycine increase . By contrast, extracellular neurotransmitter levels increase indiscriminately in anoxia-intolerant animals: dopamine, aspartate, glutamate, GABA and taurine all increase in the hypoxic or anoxic neonatal rat and adult rat brain (Huang et al, 1994;PerezPinzon et al, 1993;Young et al, 1993), while glutamate, aspartate, GABA, and taurine are all released from hippocampal slices exposed to hypoxia, chemical ischemia or hydrogen peroxide (Saransaari and Oja, 1998).…”

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confidence: 99%

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Slow death in the leopard frogRana pipiens: neurotransmitters and anoxia tolerance

Milton

Manuel

Lutz

2003

Journal of Experimental Biology

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The effects of anoxia/ischemia on the mammalian brain, and the mechanisms that promote survival or neuronal failure, have been extensively studied owing to their great significance in human pathophysiology. In brief, the mammalian brain loses ATP within minutes of oxygen deprivation, with a subsequent failure of ATP-dependent ion exchangers, the loss of ionic gradients, and membrane depolarization. Depolarization then results in a cytotoxic increase in intracellular Ca 2+ concentration, the uncontrolled release of excitatory neurotransmitters to neurotoxic levels, and subsequent neuronal death (for a review, see Lutz et al., 2003). Once temperature differences are taken into account, this scenario is in fact the characteristic response of nearly all vertebrate brains, from fish to mammals (Lutz et al., 2003). A few species, however, including turtles in the genera Trachemys and Chrysemys and fish in the genus Carassius, can survive anoxia for days at 25°C and months at temperatures below 10°C (Lutz et al., 2003). These animals are able to greatly reduce brain metabolic rates to a level where energy costs are matched by anaerobic energy production; ATP levels are thus maintained and anoxic depolarization is avoided. Specific adaptations by which the brains of the anoxia-tolerant organisms survive include a reduction in membrane ion permeability (channel arrest) (Bickler et al., 2002), the release of inhibitory neurotransmitters such as GABA and alanine , and protection against the uncontrolled release of such excitotoxic compounds as glutamate and dopamine (Milton and Lutz, 1998;Milton et al., 2002).Some frog species (Rana temporaria, Rana pipiens) demonstrate an intermediate anoxia tolerance, their brains able to survive 4-5·h without oxygen at room temperature (Knickerbocker and Lutz, 2001;Lutz and Reiners, 1997) and at least 30·h without oxygen at 5°C (Hermes-Lima and Storey, 1996). This tolerance to anoxia appears to be accomplished through an overall metabolic depression, primarily via hypoperfusion of the skeletal muscle , which allows the frog to maintain ATP levels in certain organ systems. However, unlike truly anoxia-tolerant vertebrates, the frog brain does not defend ATP levels, and when energy stores reach a critical low, (approximately 35% of normoxic levels), ion homeostatic mechanisms are compromised and extracellular K + levels While frogs such as Rana temporaria are known to withstand 4-5·h anoxia at room temperature, little is known about the neurological adaptations that permit this. Previous research has shown that changes in neuroactive compounds such as glutamate and dopamine in anoxia-sensitive (mammalian) brains follow a strikingly different pattern than is observed in truly anoxia-tolerant vertebrates such as the freshwater turtle. The present study measured changes in the levels of whole brain and extracellular amino acids, and extracellular dopamine, in the normoxic and 3-4·h anoxic frog Rana pipiens, in order to determine whether their neurotransmitter responses resemble the anoxia-vu...

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“…In vitro brain preparations of the pond turtle [Velluti et al, 1991] offer two distinctive advantages over mammalian brain slices: (i) the neurons are able to function for prolonged periods, because the brain is very resistant to hypoxia [Belkin, 1963;Sick et al, 1982;Young et al, 1993], and (ii) not being sliced, the preparation retains the intrinsic synaptic circuits and, therefore, spontaneous electrographic activity.…”

Section: Frequency Potentiation In the Medial Cortex Of Young Turtle mentioning

confidence: 99%

Frequency Potentiation in the Medial Cortex of Young Turtle Brains in vitro

Muñoz

Magariños-Ascone²,

Gaztelu³

et al. 1998

Brain Behav Evol

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Turtle brains have a relatively primitive cortex. Glutamate receptors in the cortex of turtles include N-methyl-D-aspartate (NMDA) and DL-α-amino-3-hydroxy-5-methylisoxazole-propionic acid (AMPA). Our aim was to determine whether the medial cortex in turtles, like the cortex and hippocampus in mammals exhibits frequency potentiation, a non-lasting form of synaptic plasticity, and, if so, to identify the involved receptors. Our results indicate that (1) the medial cortex exhibits this phenomenon with septal stimulation at 2 Hz, the frequency with maximum power spectral density in the electrocorticogram of turtles, showing an increase in both the excitatory postsynaptic potential and the evoked potential amplitudes; (2) the frequency potentiation of the medial cortex in turtles is mediated by AMPA type glutamate receptors; (3) the dynamics of frequency potentiation development in turtles show a number of differences from that in mammals. In summary, the cortex in this group of reptiles exhibits a functional trait of the cortex in mammals that is related to learning and memory; this trait, frequency potentiation, may have appeared as an independent specialization in both groups.

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Effect of anoxia on excitatory amino acids in brain slices of rats and turtles: in vitro microdialysis

Cited by 11 publications

References 0 publications

Characterization and Developmental Aspects of Anoxia-Induced Gasping in the Rat

Characterization and Developmental Aspects of Anoxia-Induced Gasping in the Rat

Slow death in the leopard frogRana pipiens: neurotransmitters and anoxia tolerance

Frequency Potentiation in the Medial Cortex of Young Turtle Brains in vitro

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