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

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.

Calcium currents of olfactory bulb juxtaglomerular cells: profile and multiple conductance plateau potential simulation.

The olfactory glomerulus is the locus of information transfer between olfactory sensory neurons and output neurons of the olfactory bulb. Juxtaglomerular cells (JGCs) may influence intraglomerular processing by firing plateau potentials that support multiple spikes. It is unclear what inward currents mediate this firing pattern. In previous work, we characterized potassium currents of JGCs. We focus here on the inward currents using whole cell current clamp and voltage recording in a rat in vitro slice preparation, as well as computer simulation. We first showed that sodium current was not required to mediate plateau potentials. Voltage clamp characterization of calcium current (I(Ca)) determined that I(Ca) consisted of a slow activating, rapidly inactivating (τ(10%-90% rise) 6-8 ms, τ(inactivation) 38-77 ms) component I(cat1), similar to T-type currents, and a sustained (τ(inactivation)>>500 ms) component I(cat2), likely composed of L-type and P/Q-type currents. We used computer simulation to test their roles in plateau potential firing. We robustly modeled I(cat1) and I(cat2) to Hodgkin-Huxley schemes (m(3)h and m(2), respectively) and simulated a JGC plateau potential with six conductances: calcium currents as above, potassium currents from our prior study (A-type I(kt1), D-type I(kt2), delayed rectifier I(kt3)), and a fast sodium current (I(Na)). We demonstrated that I(cat1) was required for mediating the plateau potential, unlike I(Na) and I(cat2), and its τ(inactivation) determined plateau duration. We also found that I(kt1) dictated plateau potential shape more than I(kt2) and I(kt3). The influence of these two transient and opposing conductances suggests a unique mechanism of plateau potential physiology.