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

J Physiol. 2000 Feb 1;522 Pt 3(Pt 3):427-42. doi: 10.1111/j.1469-7793.2000.00427.x.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • 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*
  • 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

Substances

  • Potassium Channel Blockers
  • Potassium Channels
  • Barium
  • Strophanthidin
  • Sodium-Potassium-Exchanging ATPase
  • Potassium