Influence of the mucosa on the excitability of myenteric neurons

Abstract

Intracellular microelectrodes were used to examine the active and passive membrane properties of neurons in the myenteric plexus of the guinea-pig small intestine. Neurons of two types were examined: S neurons, which have prominent fast excitatory postsynaptic potentials and in which action potentials are not followed by long-lasting afterhyperpolarizations, and AH neurons, which have long-lasting afterhyperpolarizations following soma action potentials. In preparations in which the myenteric ganglia and longitudinal muscle, but no mucosa, were present, most S neurons (59/64) responded to intracellular depolarizing current with brief bursts of action potentials. Regardless of the strength of a depolarizing current of 500- ms duration, these neurons never fired action potentials beyond the first 250 ms. S neurons in this state were called rapidly accommodating. In contrast, within 600 microm circumferential to the intact mucosa, 26/58 S neurons fired action potentials for most or all of the period of a 500-ms insightful depolarizing pulse. S neurons in this state were called slowly accommodating. Depolarization of S neurons in the rapidly accommodating state caused a rapidly developing reduction in membrane resistance (outward rectification; onset about 7 ms). This rectification was absent from S neurons in the slowly accommodating state. Tetraethylammonium blocked the early rectification and the changed neuronal state from rapidly accommodating to slowly accommodating. Application of tetrodotoxin to neurons in the slowly accommodating state revealed the early rectification, indicating that its absence from these neurons before tetrodotoxin was applied had been due to ongoing activity in axons providing synaptic input to the neurons. After the mucosa was disconnected from the other layers and laid back in its original position, all S neurons close to the mucosa were in the rapidly accommodating state (17/17). Slow excitatory postsynaptic potentials, evoked by electrical stimulation of nerve tracts, converted 17 of 43 S neurons from rapidly accommodating to slowly accommodating and eliminated the early outward rectification in these neurons. These results indicate that the action potential firing properties of S neurons can be changed by external influences, including the activity of synaptic inputs that release a slowly acting transmitter. Spontaneous antidromic action potentials were recorded in 8/62 AH neurons within 600 microm circumferential to the intact mucosa. It is concluded that, when the mucosa is intact, a background firing of sensory neurons occurs which leads to a state change in many S neurons innervated by the active sensory neurons. We conclude that this state change is caused by the block of a voltage-sensitive outward rectification.