Survival of energy failure in the anoxic frog brain: delayed release of glutamate.

This study investigated the relationship between energy failure and neurotransmitter release in the frog (Rana pipiens) brain during 1-3 h of anoxia. Unlike truly anoxia-tolerant species, the frog does not defend its brain energy charge. When exposed to anoxia at 25 degrees C, there is an immediate fall in brain ATP levels, which reach approximately 20% of normoxic levels in approximately 60 min. The frog, nevertheless, survives another 1-2 h of anoxia. At 100 min of anoxia, there is an increase in extracellular adenosine concentration, probably originating from the increased intracellular adenosine concentration caused by the breakdown of intracellular ATP. Increases in the levels of extracellular glutamate and GABA do not occur until 1-2 h after ATP depletion. This response is quite unlike that recorded for other vertebrates, anoxia-tolerant or anoxia-intolerant, where energy failure quickly results in an uncontrolled and neurotoxic release of excitatory neurotransmitters. In the frog, the delay in excitotoxic neurotransmitter release may be one of the factors that allow a period of survival after energy failure. Clearly, energy failure by itself is not a fatal event in the frog brain.

[1]  M. Sweeney Neuroprotective Effects of Adenosine in Cerebral Ischemia: Window of Opportunity , 1997, Neuroscience & Biobehavioral Reviews.

[2]  P. Lutz,et al.  Role for adenosine in channel arrest in the anoxic turtle brain. , 1997, The Journal of experimental biology.

[3]  P. Lutz,et al.  Contrasting strategies for anoxic brain survival--glycolysis up or down. , 1997, The Journal of experimental biology.

[4]  G. Tattersall,et al.  Hypometabolic homeostasis in overwintering aquatic amphibians. , 1997, The Journal of experimental biology.

[5]  K. Storey,et al.  Relationship between anoxia exposure and antioxidant status in the frog Rana pipiens. , 1996, The American journal of physiology.

[6]  L. Buck,et al.  Role of adenosine in NMDA receptor modulation in the cerebral cortex of an anoxia-tolerant turtle (Chrysemys picta belli). , 1995, The Journal of experimental biology.

[7]  B. Siesjö,et al.  The Biochemical Basis of Cerebral Ischemic Damage , 1995, Journal of neurosurgical anesthesiology.

[8]  B. Siesjö,et al.  Energy metabolism, ion homeostasis, and cell damage in the brain. , 1994, Biochemical Society transactions.

[9]  T. L. James,et al.  Relationship between extracellular neurotransmitter amino acids and energy metabolism during cerebral ischemia in rats monitored by microdialysis and in vivo magnetic resonance spectroscopy , 1993, Brain Research.

[10]  S. Rothman Excitotoxins: Possible Mechanisms of Action a , 1992, Annals of the New York Academy of Sciences.

[11]  P. Lutz,et al.  Release of inhibitory neurotransmitters in response to anoxia in turtle brain. , 1991, The American journal of physiology.

[12]  A. Newby Adenosine: A retaliatory metabolite , 1991 .

[13]  I. Silver,et al.  ATP and Brain Function , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[14]  R. Busto,et al.  Effect of Ischemia on the In Vivo Release of Striatal Dopamine, Glutamate, and γ‐Aminobutyric Acid Studied by Intracerebral Microdialysis , 1988, Journal of neurochemistry.

[15]  B. Siesjö Acid-base homeostasis in the brain: physiology, chemistry, and neurochemical pathology. , 1985, Progress in brain research.

[16]  B. Siesjö,et al.  Brain energy metabolism , 1978 .

[17]  D. McDougal,et al.  PHYSIOLOGICAL AND BIOCHEMICAL CHANGES IN FROG SCIATIC NERVE DURING ANOXIA AND RECOVERY 1 , 1971, Journal of neurochemistry.

[18]  H. Maker,et al.  Effect of Ischemia , 1971 .

[19]  D. McDougal,et al.  THE EFFECTS OF ANOXIA UPON ENERGY SOURCES AND SELECTED METABOLIC INTERMEDIATES IN THE BRAINS OF FISH, FROG AND TURTLE 1 , 1968, Journal of neurochemistry.

[20]  F. Rose,et al.  Anaerobiosis in a frog, Rana pipiens. , 1967, The Journal of experimental zoology.