Excitable properties and underlying Na + and K + currents in neurons from the guinea-pig jugular ganglion

Abstract

Neurons in the superior vagal (jugular) ganglion relay afferent information from thoracic visceral organs and may be important in inflammatory processes due to the peripheral release of bioactive neuropeptides such as substance P. We characterized the excitable properties and underlying voltage-gated Na + ( I Na) and K + ( I Kv) currents in acutely dissociated guinea pig jugular ganglion neurons with microelectrode and whole-cell patch-clamp recording techniques. Current clamp recordings revealed a resting potential of approx. −55 mV and input resistance of approx. 100 MΩ. Brief depolarizing steps evoked an overshooting action potential (approx. 2 ms duration), fast (< 20 ms duration) afterhyperpolarization (AHP F) sequence in all neurons, followed by a slow (> 1 s) Cd 2+-sensitive afterhyperpolarization (AHP S) in 45% of the neurons. The AHP S was implicated in limiting repetitive action potential firing during maintained depolarizing steps. The action potential in 15 17 neurons, and a major component of the whole cell I Na in 13 13 neurons were insensitive to TTX (1–10 μM), indicating that jugular neurons express predominantly a TTX-resistant type of I Na. Cd 2+ (200 μM) did not affect action potential repolarization, while tetraethylammonium (TEA; 10 mM) in the presence of Cd 2+ markedly prolonged action potential repolarization, and blocked the AHP F in 11 11 neurons. This suggested that the action potential repolarization and the AHP F are mediated by I Kv, with little contribution by Ca 2+-dependent I K ( I K(Ca). Whole cell I Kv activated rapidly (τ < 1.5 ms), and inactivated variably over a time period of seconds. I Kv activation and inactivation voltage dependencies and TEA sensitivity were compatible with its availability during the action potential and AHP F. Only 1 26 neurons exhibited current with the rapid inactivation kinetics and voltage-dependencies characteristic of classic I A-type current. These results highlight differences in the properties of jugular neurons (e.g., deficiency of rapid I A, and lack of a TTX-sensitive subpopulation), relative to those known for other visceral and somatic afferents, and thus provide a basis for further functional studies.