Intracellular study of tonic-type enteric neurons in guinea pig small intestine

Abstract

Intracellular recording revealed a population of myenteric neurons with electrical behavior that appeared equivalent to the tonic-type mechanosensitive neurons found in earlier studies that utilized extracellular recording of single units. Electrical stimulation of the interganglionic fiber tracts evoked a slowly rising excitatory postsynaptic potential (slow EPSP) that was prolonged for several seconds after termination of the stimulus in these cells. The somal membranes had relatively low excitability in the absence of fiber tract stimulation. This was indicated by: failure of depolarizing current pulses to elicit spike discharge in some cells; when spikes were elicited by depolarizing current pulses, 1-3 spikes occurred and these were seen only at the onset of the pulse; passive invasion of the soma by current from spikes in the cell''s processes did not trigger spikes; the spikes were followed by prolonged hyperpolarizing afterpotentials associated with decreased input resistance. Characteristics of the augmented excitability during the slow EPSP were: endogenous discharge of trains of spikes; spike discharge throughout 200 ms duration depolarizing current pulses; electrotonic spike potentials from the processes triggered by somal spikes; and, postspike afterhyperpolarization was reduced or abolished. The slow EPSP was reduced or abolished in Krebs solution with 16 mM Mg2+ and in Hepes[4-(2-hydroxyethyl)-1-piperazine-N''-2-ethanesulfonic acid]-buffered Krebs with 1 mM Mn2+. It was enhanced in Krebs solution with 3 times normal Ca2+. Spike discharge in elevated Ca2+ eliminated the increase in input resistance associated with the slow EPSP. Ca availability was an important factor in regulation of membrane conductance and excitability in the perikaryon. The slow EPSP provides a mechanism whereby the soma of a multipolar neuron gates the spread of excitation between its dendrites and axon.