Activity-dependent extracellular K+ accumulation in rat optic nerve: the role of glial and axonal Na+ pumps.
1. We measured activity-dependent changes in [K+]o with K(+)-selective microelectrodes in adult rat optic nerve, a CNS white matter tract, to investigate the factors responsible for post-stimulus recovery of [K+]o. 2. Post-stimulus recovery of [K+]o followed a double-exponential time course with an initial, fast time constant, tau fast, of 0.9 +/- 0.2 s (mean +/- S.D.) and a later, slow time constant, tau slow, of 4.2 +/- 1 s following a 1 s, 100 Hz stimulus. tau fast, but not tau slow, decreased with increasing activity-dependent rises in [K+]o. tau slow, but not tau fast, increased with increasing stimulus duration. 3. Post-stimulus recovery of [K+]o was temperature sensitive. The apparent temperature coefficients (Q10, 27-37 degrees C) for the fast and slow components following a 1 s, 100 Hz stimulus were 1.7 and 2.6, respectively. 4. Post-stimulus recovery of [K+]o was sensitive to Na+ pump inhibition with 50 microM strophanthidin. Following a 1 s, 100 Hz stimulus, 50 microM strophanthidin increased tau fast and tau slow by 81 and 464%, respectively. Strophanthidin reduced the temperature sensitivity of post-stimulus recovery of [K+]o. 5. Post-stimulus recovery of [K+]o was minimally affected by the K+ channel blocker Ba2+ (0.2 mM). Following a 10 s, 100 Hz stimulus, 0.2 mM Ba2+ increased tau fast and tau slow by 24 and 18%, respectively. 6. Stimulated increases in [K+]o were followed by undershoots of [K+]o. Post-stimulus undershoot amplitude increased with stimulus duration but was independent of the peak preceding [K+]o increase. 7. These observations imply that two distinct processes contribute to post-stimulus recovery of [K+]o in central white matter. The results are compatible with a model of K+ removal that attributes the fast, initial phase of K+ removal to K+ uptake by glial Na+ pumps and the slower, sustained decline to K+ uptake via axonal Na+ pumps.
Ransom
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Department of Neurobiology, University of Alabama School of Medicine, Birmingham 35294, USA.
Ransom
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Sontheimer
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D000818:Animals; D001369:Axons / Q000378:metabolism*; D001464:Barium / Q000494:pharmacology; D046508:Culture Techniques; D004558:Electric Stimulation; D005110:Extracellular Space / Q000378:metabolism*; D008297:Male; D008839:Microelectrodes; D009457:Neuroglia / Q000166:cytology / Q000378:metabolism*; D009900:Optic Nerve / Q000166:cytology / Q000187:drug effects / Q000378:metabolism*; D011188:Potassium / Q000378:metabolism*; D026902:Potassium Channel Blockers; D015221:Potassium Channels / Q000378:metabolism; D051381:Rats; D020318:Rats, Long-Evans; D000254:Sodium-Potassium-Exchanging ATPase / Q000037:antagonists & inhibitors / Q000378:metabolism*; D013327:Strophanthidin / Q000494:pharmacology; D013696:Temperature; D013997:Time Factors
D026902:Potassium Channel Blockers; D015221:Potassium Channels; D001464:Barium; D013327:Strophanthidin; D000254:Sodium-Potassium-Exchanging ATPase; D011188:Potassium