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

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Abstract
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, τfast, of 0.9 ± 0.2 s (mean ±s.d.) and a later, slow time constant, τslow, of 4.2 ± 1 s following a 1 s, 100 Hz stimulus. τfast, but not τslow, decreased with increasing activity-dependent rises in [K+]o. τslow, but not τfast, increased with increasing stimulus duration. Post-stimulus recovery of [K+]o was temperature sensitive. The apparent temperature coefficients (Q10, 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 τfast and τslow 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 Ba2+ (0.2 mm). Following a 10 s, 100 Hz stimulus, 0.2 mm Ba2+ increased τfast and τslow 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.