Bursts of action potentials and intrinsic sensory neurons of the intestine

Abstract

The pattern of input to intestinal sensory neurons shapes their output and is, thus, fundamental to an understanding of the initiation and propagation of intestinal reflexes. Recent data suggests that this input consists largely of bursts of action potentials (APs). We investigated the origin of these bursts in 60 ileal sensory neurons taken from guinea pigs that were stunned by a blow to the head and killed by severing the carotid arteries. All myenteric neurons were near intact mucosa and intracellular electrophysiological recording techniques were used during selective electrical stimulation of the mucosal epithelium and of the cell body. Three types of bursts were seen: following an antidromic AP evoked by electrical stimulation of the mucosa (66% of neurons); following an AP evoked at the soma (30%); and spontaneously occurring (38%). All bursts had an average intra-burst frequency of 50 Hz and all tended to occur in the same population of neurons. All APs in a burst persisted during somatic hyperpolarization and many had an inflection on their rising phase. They also persisted in low calcium solutions and a variety of ligand-gated ion channel receptor antagonists. TTX (300 nM) abolished all bursts while TTX (30 nM), tropisetron (30 microM) or a high calcium, high magnesium solution selectively blocked the later APs in a burst. Results from collision experiments suggest that both the electrically and somatically evoked bursts originate near the sensory nerve terminals in the mucosa. The characteristics of the bursts of APs are common, suggesting a common mechanism underlies each. This involves positive feedback between nerve terminals and epithelial elements and may be important in differentiating or integrating sensory modalities.