A voltage-clamp study of the electrophysiological characteristics of the intramural neurones of the rat trachea.

1. The electrophysiological characteristics of intramural neurones from the paratracheal ganglia of 14- to 18-day-old rats were studied in vitro using intracellular, single-electrode current- and voltage-clamp techniques. 2. Resting membrane potentials ranged between -50 and -73 mV. In 50-60% of all neurones, random and occasionally patterned bursts of spontaneous, fast synaptic potentials were observed. In all cases, superfusion with either hexamethonium (100 microM), or Ca2(+)-free, high-magnesium-containing solutions abolished all synaptic activity. 3. Two distinct patterns of spike discharge were observed in response to prolonged intrasomal current injection. Most cells (65-75%) fired rhythmic, high-frequency (50-90 Hz) bursts of action potentials, with interburst intervals of between 300 and 500 ms, throughout the period of current stimulation. A further 10-15% of cells fired tonically at low frequencies (10-15 Hz) for the duration of the applied stimulus. In both cell types, trains of action potentials were followed by a pronounced calcium-dependent after-hyperpolarization which persisted for up to 3 s. The magnitude of the after-hyperpolarization following a single spike in tonic-firing cells was considerably larger than in burst-firing cells. Both the action potential and the after-hyperpolarization in all cells displayed a calcium-dependent, tetrodotoxin-resistant component which was abolished by the removal of the extracellular calcium. 4. The spike after-hyperpolarization resulted from activation of an outward calcium-dependent potassium current which reversed at -86.5 mV. This value was shifted by 63.6 mV for a 10-fold increase in extracellular potassium concentration. 5. All of the cells studied exhibited marked outward rectification when depolarized. This resulted from activation of a time- and voltage-dependent M-current. The slow inward current relaxations associated with the M-current became faster at more negative potentials and reversed around -85 mV. Raising the extracellular potassium concentration shifted the reversal potential for the current relaxations to more depolarized potentials in a manner predicted by the Nernst equation for a current carried by potassium ions. Both the outward current at depolarized potentials and the slow current relaxations were potently inhibited by extracellular BaCl2 (1 mM) but were unaffected by CsCl (1-3 mM). 6. Inward rectification at hyperpolarized potentials was a characteristic of all cells. Membrane hyperpolarization revealed inward rectification in the 'instantaneous' current-voltage relationship at membrane potentials greater than -80 mV.(ABSTRACT TRUNCATED AT 400 WORDS)