Primary involvement of K+ conductance in membrane resonance of trigeminal root ganglion neurons

Abstract

1. The complex impedances and impedance magnitude functions were obtained from neurons in in vitro slices of trigeminal root ganglia using frequency-domain analyses of intracellularly recorded voltage responses to specified oscillatory input currents. A neuronal model derived from linearized Hodgkin-Huxley-like equations was used to fit the complex impedance data. This procedure yielded estimates for membrane electrical properties. 2. Membrane resonance was observed in the impedance magnitude functions of all investigated neurons at their initial resting membrane potentials and was similar to that reported previously for trigeminal root ganglion neurons in vivo. Tetrodotoxin (10(-6) M), a Na+-channel blocker, applied in the bathing medium for 20 min produced only minor changes, if any, in the resonance, although gross impairment of Na+-spike electrogenesis was apparent in most of the neurons. Brief applications (1-5 min) of a K+-channel blocker, tetraethylammonium (TEA; 10(-2) M), increased the impedance magnitude and abolished, in a reversible manner, the resonant behavior. In all cases, the resonant frequency was decreased by TEA administration prior to total blockade of resonance. 3. The TEA-induced blockade of resonance was associated with decreases in the estimates of the membrane conductances, without significant alterations of input capacitance. A particularly large decrease was observed in Gr, the time-invariant resting conductance that includes a lumped leak conductance component. The voltage- and time-dependent conductance, GL, and associated relaxation time constant, tau u, also declined progressively during administration of TEA. 4. Systematic variations in the membrane potentials of trigeminal root ganglion neurons were produced by intracellular injections of long-lasting step currents with superposition of the oscillatory current stimuli, in order to assess the effects of TEA on the relationship of the electrical properties to the membrane potential. Applications of TEA led to a depolarizing shift in the dependence of the membrane property estimates, suggesting voltage-dependence of the effects of TEA on presumed K+ channels in the membrane. 5. These data suggest a primary involvement of K+ conductance in the genesis of membrane resonance. This electrical behavior or its ionic mechanism is a major modulator of the subthreshold electrical responsiveness of trigeminal root ganglion neurons.

Multiple Interacting Sites of Ectopic Spike Electrogenesis in Primary Sensory Neurons

“…At 1 mM, 4-AP also partially blocks the slowly inactivating K ϩ conductance I D (Everill et al, 1998;Fedulova et al, 1998). Finally, our data resolve an anomaly in observations by Puil et al (1988Puil et al ( , 1989 in trigeminal ganglion (TRG) neurons. In their study, 4-AP suppressed membrane resonance in the cell soma but nevertheless enhanced spiking.…”

Development of Inward Rectification and Control of Membrane Excitability in Mesencephalic V Neurons

“…Frequency-domain analysis (Puil et al 1986(Puil et al , 1988 was performed by injecting a computer generated ZAP input current of changing frequencies between 0 and 250 Hz into neurons around or more negative to resting potential and recording the resulting voltage responses. To carefully analyze the subthreshold membrane properties in the absence of spikes, the amplitude of the ZAP input function was adjusted to keep the peak-to-peak voltage responses smaller than 10 mV.…”

Resonant or Not, Two Amplification Modes of Proprioceptive Inputs by Persistent Inward Currents in Spinal Motoneurons

“…We used the impedance amplitude profile (ZAP) method to characterize the resonant behavior of the cells (Puil et al, 1988;Hutcheon and Yarom, 2000). We generated a sine wave current I ZAP (t) ϭ a ϫ sin(bt k ) of 10 s with the Power1401.…”