Bursts of recurrent excitation in the activation of intrinsic sensory neurons of the intestine

Abstract

Sensory neurons intrinsic to the wall of the intestine receive input from stimuli in the lumen. These stimuli interact with the mucosal epithelium causing release of sensory mediators that depolarize the sensory nerve terminals. The depolarization and the subsequent pattern of action potential (AP) discharge controls the type and magnitude of the reflex evoked. The characteristics of this AP discharge were investigated in 60 intrinsic sensory neurons from the myenteric plexus of the guinea-pig ileum.

Intracellular electrophysiological recordings were made from neurons near intact mucosa during electrical stimulation of the mucosa and/or neuronal soma. Most neurons (87%) responded to mucosal stimulation with a burst of 3.8±0.3 APs (average instantaneous frequency, ƒINT 39±4 Hz). In 38%, a somatically evoked AP triggered a similar burst of 2.9±0.3 APs (ƒINT 52±6 Hz) while in 50% of neurons, there was ongoing spontaneous bursting (3.8±0.2 APs, ƒINT 48±6 Hz). APs in all of these bursts had an inflection on the rising phase and they persisted during somatic hyperpolarization indicating they were generated in a distal process rather than the soma. Collision experiments confirmed this and suggested that bursts originated near the mucosal sensory nerve terminals. A reduction in membrane excitability reduced the number of APs in a burst suggesting a brief depolarizing event, such as a voltage- or ligand-gated ion channel, was responsible.

Bursting behavior in the intrinsic sensory neurons is common for mucosal stimuli and may involve a novel transmitter acting at the sensory nerve terminal. Further, some bursting involves positive feedback between the nerve terminals and other elements in the epithelium. This is a novel and potentially important component of intestinal sensory transduction.