Passive and active (voltage- and time-dependent) membrane properties of trigeminal root ganglion neurons of decerebrate guinea pigs have been determined using frequency-domain analyses of small-amplitude perturbations of membrane voltage. The complex impedance functions of trigeminal ganglion neurons were computed from the ratios of the fast Fourier transforms of the intracellularly recorded voltage response from the neuron and of the input current, which had a defined oscillatory waveform. The impedance magnitude functions and corresponding impedance locus diagrams were fitted with various membrane models such that the passive and active properties were quantified. The complex impedances of less than one-quarter of the 105 neurons which were investigated extensively could be described by the complex impedance function for a simple RC-electrical circuit. In such neurons, the voltage responses to constant-current pulses, using conventional bridge-balance techniques, could be fitted with single exponential curves, also suggesting passive membrane behavior. A nonlinear least-squares fit of the complex impedance function for the simple model to the experimentally observed complex impedance yielded estimates of the resistance of the electrode, and of input capacitance (range, 56 to 490 pF) and input resistance (range, 0.8 to 30 M omega) of the neurons. The majority of trigeminal ganglion neurons were characterized by a resonance in the 50- to 250-Hz bandwidth of their impedance magnitude functions. Such neurons when injected with "large" hyperpolarizing current pulses using bridge-balance techniques showed membrane voltage responses that "sagged" (time-dependent rectification). Also, repetitive firing commonly occurred with depolarizing current pulses; this characteristic of neurons with resonance in their impedance magnitude functions was not observed in neurons with "purely" passive membrane behavior. A nonlinear least-squares fit of a five-parameter impedance fitting function based on a membrane model to the impedance locus diagram of a neuron with resonance yielded estimates of its membrane properties: input capacitance, the time-invariant part of the conductance, the conductance activated by the small oscillatory input current, and the relaxation time constant for this conductance. The ranges of the estimates for input capacitance and input resistance were comparable to the ranges of corresponding properties derived for neurons exhibiting "purely" passive behavior.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

The electrical impedance of trigeminal ganglion cells (in vivo) and hippocampal CA1 neurons (in vitro) of guinea pigs was measured in the frequency range of 5-1250 Hz using intracellular recording techniques with single microelectrodes and computerized methodology. The transfer functions of the electrode and the electrode-neuron system were computed from the ratio of fast Fourier transforms of the output voltage response from the neuron and input current composed of sine waves with rapidly increasing frequency which displaced membrane potential by 2-5 mV. We believe these to be the first measurements of complex impedance and transfer functions in peripheral and central neurons of vertebrates and the first use of such input current functions. The majority of trigeminal ganglion cells did not exhibit electrical behaviour ascribable to a simple resistance-capacitance (RC) circuit but showed a hump at low frequencies (5-250 Hz) in the computed transfer function, probably attributable to resonance. The transfer function in less than 20% of the trigeminal neurons could be fitted approximately to a theoretical transfer function (resistance in series with a parallel RC circuit model) providing values for electrode resistance, effective input resistance, and effective input capacitance. The transfer functions measured in hippocampal CA1 neurons were characterized by a rapid fall-off in the low frequency range (less than 200 Hz). Impedance locus plots approximate the locus corresponding to a series RC circuit in parallel with a parallel RC circuit.

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1. The effects of general anesthesia on passive and active membrane properties of trigeminal root ganglion neurons of decerebrate guinea pigs have been determined using frequency-domain analyses of small-amplitude perturbations of membrane voltage. Quantification of the effects was accomplished by fitting the complex impedance locus diagrams computed from the neuronal responses with a membrane model based on linearized Hodgkin-Huxley-like equations. 2. Endotracheal administrations of isoflurane (2-3% for periods of 30-180 s), the most extensively studied of five general anesthetics, did not elicit large changes in membrane potential or in electrical properties in 26 of the 38 neurons. In this relatively unresponsive group, application of isoflurane in higher concentrations (3-4%) tended to evoke small but significant changes (less than 20%) in membrane properties without altering membrane potential by greater than 5 mV. These changes consisted of increases in the effective input capacitance and input conductance. 3. The impedance magnitude functions were reduced in amplitude consistently in 12 of the 38 neurons during induction of general anesthesia with isoflurane (2-4%) or, in several cases, with halothane (2%). Such applications evoked depolarizations of 8-32 mV, which also were observed in several instances of anesthesia with enflurane and cyclopropane. Quantification of these effects on electrical properties by curve fitting with the linearized Hodgkin-Huxley model revealed increases in the effective input capacitance, in the time-invariant resting conductance, Gr, and in the voltage- and time-dependent conductance, GL. Sometimes, an initial decrease preceded the increase of Gr, and the relaxation time constant associated with GL usually was reduced by the anesthetic agent in the 12 neurons. 4. In 10 neurons, membrane resonance behavior (which was apparent as a large hump at low frequencies of the impedance magnitude functions) was reduced in amplitude, as well as broadened in bandwidth, when peak changes in membrane properties were evident, i.e., during surgical or deep anesthesia. These actions of isoflurane or halothane were correlated to a reduction in spike electrogenesis and they may account for the reduced tendency of neurons to fire repetitive action potentials during anesthesia with isoflurane or halothane.(ABSTRACT TRUNCATED AT 400 WORDS)