Unable to compromise on its intense energy consumption, most vertebrate brains go into energy failure within minutes of being deprived of oxygen,resulting in the loss of ionic gradients, depolarization and a cascade of pathological changes resulting eventually in neuronal death. A few vertebrate species, however, including freshwater turtles of the genera Trachemys and Chrysemys, have brains able to survive at least 48 h of anoxia at 25°C and up to 3-4 months during winter hibernation in frozen ponds. The animals are able to tolerate such long periods without oxygen by lowering energy metabolism to a bare minimum, where brain energy needs can be fully met by anaerobic glycolysis. As a result, the turtle brain is able to maintain ATP levels and ionic gradients during anoxia and thus avoid the fatal consequences of energy failure.

Among other adaptations, one means by which this balance of decreased ATP production and energy utilization can be achieved is by a reduction in membrane ion permeability, termed channel arrest, which provides important energy savings for the anoxia-tolerant brain by reducing the costs of ion pumping to maintain homeostasis. Previous studies have indicated a significant and acute decrease in whole-cell conductance during anoxia, which is the result of decreased potassium flux, a decrease in the density of voltage-gated Na+ channels and a downregulation of NMDA receptor calcium channels; these reductions in ion leakage permit a simultaneous decrease in Na+/K+-ATPase activity to conserve ATP. But besides decreases in ion leakage currents, another potential way to save energy is by changing neuronal gap junction permeability, a possibility addressed by Shin and co-workers in their recent Comparative Biochemistry and Physiology A paper. Gap junctions are structural elements present in a variety of vertebrate and invertebrate tissues that provide a low-resistance, high-speed pathway between adjacent cells.

Les Buck and his group measured whole cell capacitance in normoxic and anoxic cortical sheets from the turtle Chrysemys picta under a variety of conditions known to affect gap junction permeability, including high calcium, hypo-osmotic shock, cold shock and exposure to a variety of neuroactive compounds including isoproterenol, a nitric oxide donor, and adenosine. To visually inspect whether gap junction permeability changed in the turtle brain, neurons were loaded with Lucifer yellow, a dye that shows gap junction coupling to adjacent cells.

Anoxia alone did not change cellular capacitance, nor did calcium or adenosine perfusion, although decreases in whole-cell conductance were observed under these conditions. In fact, perfusion with hypo-osmotic artificial cerebrospinal fluid was the only protocol consistently altering capacitance, and that was in the direction of an apparent decrease in gap junction permeability, resulting in reduced cell-to-cell communication. While it was determined that gap junctions were present in the turtle cortex, they proved to be very difficult to open, leading the researchers to conclude that decreases in cellular conductance are due almost exclusively to decreases in leak channel permeability, rather than any changes in gap junctions, and that the possession of very low permeability gap junctions may be another identifying characteristic of a good vertebrate facultative anaerobe.

References

Shin, D. S., Ghai, H., Cain, S. W. and Buck, L. T.(
2003
). Gap junctions do not underlie changes in whole cell conductance in anoxic turtle brain.
Comp. Biochem. Physiol. A
134
,
181
-194.