Activity-dependent extracellular K+ accumulation in rat optic nerve: the role of glial and axonal Na+ pumps

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 . Post-stimulus recovery of [K + ] o followed a double-exponential time course with...

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Bibliographic Details
Published in:The Journal of physiology 2000-02, Vol.522 (3), p.427-442
Main Authors: Ransom, Christopher B., Ransom, Bruce R., Sontheimer, Harald
Format: Article
Language:English
Subjects:
Animals
Axons - metabolism
Barium - pharmacology
Culture Techniques
Electric Stimulation
Extracellular Space - metabolism
Male
Microelectrodes
Neuroglia - cytology
Neuroglia - metabolism
Optic Nerve - cytology
Optic Nerve - drug effects
Optic Nerve - metabolism
Original
Potassium - metabolism
Potassium Channel Blockers
Potassium Channels - metabolism
Rats
Rats, Long-Evans
Sodium-Potassium-Exchanging ATPase - antagonists & inhibitors
Sodium-Potassium-Exchanging ATPase - metabolism
Strophanthidin - pharmacology
Temperature
Time Factors
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Summary: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 . Post-stimulus recovery of [K + ] o followed a double-exponential time course with an initial, fast time constant, τ fast , of 0.9 ± 0.2 s (mean ± s.d. ) and a later, slow time constant, τ slow , of 4.2 ± 1 s following a 1 s, 100 Hz stimulus. τ fast , but not τ slow , decreased with increasing activity-dependent rises in [K + ] o . τ slow , but not τ fast , increased with increasing stimulus duration. Post-stimulus recovery of [K + ] o was temperature sensitive. The apparent temperature coefficients ( Q 10 , 27–37°C) for the fast and slow components following a 1 s, 100 Hz stimulus were 1.7 and 2.6, respectively. Post-stimulus recovery of [K + ] o was sensitive to Na + pump inhibition with 50 μM strophanthidin. Following a 1 s, 100 Hz stimulus, 50 μM strophanthidin increased τ fast and τ slow by 81 and 464%, respectively. Strophanthidin reduced the temperature sensitivity of post-stimulus recovery of [K + ] o . Post-stimulus recovery of [K + ] o was minimally affected by the K + channel blocker Ba 2+ (0.2 m m ). Following a 10 s, 100 Hz stimulus, 0.2 m m Ba 2+ increased τ fast and τ slow by 24 and 18%, respectively. 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. 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.
ISSN:0022-3751
1469-7793
DOI:10.1111/j.1469-7793.2000.00427.x