Afterspike-hyperpolarization of neurons in the inferior mesenteric ganglion in guinea-pig

Abstract

Intracellular recordings were made from neurons ( n = 121) in the inferior mesenteric ganglion (IMG) in guinea-pig. The afterspike hyperpolarization (ASH) following a single action potential was studied in IMG cells which received an excitatory, cholinergic innervation from mechanosensory nerves in the gastrointestinal tract. The amplitude of ASH was dependent on the membrane potential of IMG cells and the concentration of K + in the bathing solution. The reversal potential of ASH (−80–−90 mV, in normal Krebs solution) appeared to follow the equilibrium potential for K +, as [K +] o was changed, suggesting that ASH was the product of K +-efflux. Further evidence suggested that a major component of the K +-efflux was dependent on the concentration of Ca 2+ in the bathing medium. Elevation and reduction of [Ca 2+] o increased and decreased, respectively, the amplitude and duration of ASH. In the presence of tetrodotoxin, depolarizing current pulses elicited spike-like events which (1) were dependent on [Ca 2+] o and the degree of depolarization by current-clamp and (2) were followed by afterhyperpolarizations that were also dependent on [Ca 2+] o and degree of depolarization by current-clamp. In the combined presence of tetrodotoxin and tetraethylammonium, depolarizing current pulses elicited prolonged action potentials (up to 100 ms in duration) followed by prolonged ASH (up to 3 s in duration). Spike-like events, prolonged action potentials and their afterhyperpolarizations were reduced in amplitude and duration when the calcium-channel blocking ion, Co 2+, or blocking drug, verapamil, was present in the bathing medium. In normal Krebs solution, the ASH of action potentials produced by nerve stimulation was reduced but not abolished in the presence of Co 2+. These results suggested that Ca 2+ entered IMG cells during depolarization and activated the K +-conductance mechanisms responsible for the ASH. However, an initial component of the ASH may have involved other voltage-dependent K +-currents known to be activated during the excitation of sympathetic neurons [1]. The amplitude and duration of ASH differed during non-synaptic and synaptic excitation of IMG cells, and differed when action potentials resulted from fast and slow EPSPs. In addition, the amplitude and duration of ASH were altered by noradrenaline, by the cholinomimetic, carbachol, and by 3 neuropeptides present in the IMG, namely leucine-enkephalin, substance P and vasoactive intestinal polypeptide. Since the amplitude and duration of the ASH influences the duration of the interspike interval, the signal output of the IMG may depend on the manner in which IMG cells are excited and the nature of the transmitters involved.