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

* We measured activity-dependent changes in [K super(+)] sub(o) with K super(+)-selective microelectrodes in adult rat optic nerve, a CNS white matter tract, to investigate the factors responsible for post-stimulus recovery of [K super(+)] sub(o). * Post-stimulus recovery of [K super(+)] sub(o) foll...

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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
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Summary:* We measured activity-dependent changes in [K super(+)] sub(o) with K super(+)-selective microelectrodes in adult rat optic nerve, a CNS white matter tract, to investigate the factors responsible for post-stimulus recovery of [K super(+)] sub(o). * Post-stimulus recovery of [K super(+)] sub(o) followed a double-exponential time course with an initial, fast time constant, tau sub(fast), of 0.9 plus or minus 0.2 s (mean plus or minus s.d.) and a later, slow time constant, tau sub(slow), of 4.2 plus or minus 1 s following a 1 s, 100 Hz stimulus. tau sub(fast), but not tau sub(slow), decreased with increasing activity-dependent rises in [K super(+)] sub(o). tau sub(slow), but not tau sub(fast), increased with increasing stimulus duration. * Post-stimulus recovery of [K super(+)] sub(o) was temperature sensitive. The apparent temperature coefficients (Q sub(10), 27-37 degree 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 super(+)] sub(o) was sensitive to Na super(+) pump inhibition with 50 mu M strophanthidin. Following a 1 s, 100 Hz stimulus, 50 mu M strophanthidin increased tau sub(fast) and tau sub(slow) by 81 and 464%, respectively. Strophanthidin reduced the temperature sensitivity of post-stimulus recovery of [K super(+)] sub(o). * Post-stimulus recovery of [K super(+)] sub(o) was minimally affected by the K super(+) channel blocker Ba super(2+) (0.2 mm). Following a 10 s, 100 Hz stimulus, 0.2 mm Ba super(2+) increased tau sub(fast) and tau sub(slow) by 24 and 18%, respectively. * Stimulated increases in [K super(+)] sub(o) were followed by undershoots of [K super(+)] sub(o). Post-stimulus undershoot amplitude increased with stimulus duration but was independent of the peak preceding [K super(+)] sub(o) increase. * These observations imply that two distinct processes contribute to post-stimulus recovery of [K super(+)] sub(o) in central white matter. The results are compatible with a model of K super(+) removal that attributes the fast, initial phase of K super(+) removal to K super(+) uptake by glial Na super(+) pumps and the slower, sustained decline to K super(+) uptake via axonal Na super(+) pumps.
ISSN:0022-3751
1469-7793
DOI:10.1111/j.1469-7793.2000.00427.x