Brain sensitivity to anoxia in fish as reflected by changes in extracellular K+ activity

Most vertebrates have a very limited tolerance to anoxia. The only exceptions to this rule are found among ectothermic species, notably crucian carp (Carassius carassius) and freshwater turtles. It has been assumed that the brains of these species are less sensitive to anoxia than ectothermic brains in general. However, it has not been possible to exclude that anoxia-intolerant species like rainbow trout (Oncorhynchus mykiss) die from heart failure rather than brain failure during anoxia, and that the average ectothermic brain is actually rather insensitive to anoxia. By simultaneously measuring the effect of anoxia on brain extracellular K+ activity ([K+]o), blood pressure, and heart rate in rainbow trout, we show that the rainbow trout brain rapidly loses ion homeostasis during anoxia, despite an initial increase in blood pressure. The rainbow trout brain showed a sudden transient increase in [K+]o (suggesting a rapid depolarization) after approximately 30 min of anoxia at 10 degrees C. At the same time the blood pressure was still close to the normoxic value. In a comparative experiment, crucian carp was found to maintain a low brain [K+]o for at least 6 h of anoxia. Thus the results suggest that the rainbow trout brain is anoxia-intolerant in itself, and that its ability to maintain ion gradients during anoxia is very much lower than that of crucian carp. If temperature differences are taken into account, the anoxia sensitivity of the rainbow trout brain is comparable to that of mammals.