Potassium currents of olfactory bulb juxtaglomerular cells: characterization, simulation, and implications for plateau potential firing

Neuroscience. 2011 Sep 29;192:247-62. doi: 10.1016/j.neuroscience.2011.06.012. Epub 2011 Jun 13.

Abstract

Odor identity is encoded by the activity of olfactory bulb glomeruli, which receive primary sensory input and transfer it to projection neurons. Juxtaglomerular cells (JGCs) may influence glomerular processing via firing of long lasting plateau potentials. Though inward currents have been investigated, little is known regarding potassium current contribution to JGC plateau potentials. We pursued study of these currents, with the overarching goal of creating components for a computational model of JGC plateau potential firing. In conditions minimizing calcium-activated potassium current (I(K(Ca))), we used whole cell voltage clamp and in vitro slice preparations to characterize three potassium currents in rat JGCs. The prominent component I(kt1) displayed rapid kinetics (τ(10%-90% rise), 0.6-2 ms; τ(inactivation), 5-10 ms) and was blocked by high concentration 4-aminopyridine (4-AP) (5 mM) and tetramethylammonium (TEA) (40 mM). It had half maximal activation at -10 mV (V(½)max) and little inactivation at rest. I(kt2), with slower kinetics (τ(10%-90% rise), 11-15 ms; τ(inactivation), 100-300 ms), was blocked by low concentration 4-AP (0.5 mM) and TEA (5 mM). The V(½)max was 0 mV and inactivation was also minimal at rest. Sustained current I(kt3) showed sensitivity to low concentration 4-AP and TEA, and had V(½)max of +10 mV. Further experiments, in conditions of physiologic calcium buffering, suggested that I(K(Ca)) contributed to I(kt3) with minimal effect on plateau potential evolution. We transformed these characterizations into Hodgkin-Huxley models that robustly mimicked experimental data. Further simulation demonstrated that I(kt1) would be most efficiently activated by plateau potential waveforms, predicting a critical role in shaping JGC firing. These studies demonstrated that JGCs possess a unique potassium current profile, with delayed rectifier (I(kt3)), atypical A-current (I(kt1)), and D-current (I(kt2)) in accordance with known expression patterns in olfactory bulb (OB) glomeruli. Our simulations also provide an initial framework for more integrative models of JGC plateau potential firing.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Membrane Potentials / physiology*
  • Models, Neurological*
  • Neurons / metabolism*
  • Olfactory Bulb / metabolism*
  • Organ Culture Techniques
  • Patch-Clamp Techniques
  • Potassium / metabolism*
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Potassium