Changes in turtle brain neurotransmitters and related substances during anoxia

Abstract

Freshwater turtles (Pseudemys scripta elegans) were exposed to 0.5-13 h of anoxia at 25 degrees C, whereupon the brain concentrations of 14 amino acid and monoamine neurotransmitters and related substances were measured. Monoamines are of particular interest, because their synthesis and (in part) degradation require molecular oxygen. During anoxia, the level of the inhibitory transmitter gamma-aminobutyric acid (GABA) increased (2.3-fold after 13 h) and the level of the excitatory transmitter Glu fell. Furthermore, anoxia caused increases in the levels of Ala (14 times after 13 h), Tau, Gly, and Ser, whereas the Gln level fell. The increase in Ala is likely to inhibit pyruvate kinase, thereby mediating the decreased rate of glycolysis seen after prolonged anoxia. The increased level of Tau might protect the turtle brain against Ca2(+)-mediated anoxic damage. The monoamine metabolites almost vanished within a few hours of anoxia, indicating a halt in monoamine synthesis and breakdown, and the dopamine level fell. Nevertheless, serotonin, norepinephrine, and epinephrine levels were maintained during 13 h of anoxia, at levels extremely high compared with mammals, suggesting adaptive mechanisms such as stockpiling. It is hypothesized that the pattern of change in levels of amino acids (notably GABA and Glu) and monoamines is of functional significance, because it promotes the decrease in brain activity and energy consumption seen in anoxic turtles.

Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark

“…In addition, hypoxia-tolerant species, as mentioned, show a neuroprotective increase in GABA levels (Nilsson, 1990;Nilsson et al, 1990Nilsson and Lutz, 1993). Histological staining for glutamate in epaulette shark brain (Fig.·4A) indicates that glutamate homeostasis is either maintained or significantly lowered in descending axon tracts such as the median longitudinal fasciculus and the fasciculus of Steida in the brainstem after exposure to hypoxia (5% of air saturation; G. Wise and G. M. C. Renshaw, unpublished observations).…”

Endothelial cell tolerance to hypoxia. Potential role of purine nucleotide phosphates.

“…The ability to tolerate acute hypoxia and, in some cases, to adapt to chronic hypoxia is critical to their survival; however, it varies greatly among different cell types. For example, many invertebrates and lower vertebrates have developed a remarkable tolerance to hypoxia (1)(2)(3)(4); in contrast, most mammalian cells and organ-isms have limited strategies for coping with oxygen depletion and are, consequently, relatively hypoxia sensitive. Yet, even among mammalian cells, there is a marked difference in sensitivity to hypoxia.…”

Effects of anoxia exposure and aerobic recovery on metabolic enzyme activities in the freshwater turtle <i>Trachemys scripta elegans</i>

“…One negative effect of oxygen deprivation on mammalian brain is the release of high levels of the excitatory amino acids glutamate and aspartate into the extracellular fluid (Young et al 1993). Turtles do not show this; in fact, both extracellular glutamate (Young et al 1993) and total brain glutamate (Nilsson et al 1990) decreased significantly during anoxia, whereas levels of inhibitory amino acids (g-aminobutyric acid, glycine, taurine, alanine) increased in anoxic turtle brain (Nilsson et al 1990). Although GDH participates in both glutamate synthesis and catabolism, the 57% reduction in GDH activity in turtle brain in anoxia could reduce the rate of glutamate production, leading to lower glutamate levels.…”