Synaptic responses evoked by mechanical stimulation of the mucosa in morphologically characterized myenteric neurons of the guinea-pig ileum

Abstract

Recordings were made from myenteric neurons of the guinea-pig ileum during reflexes evoked by mechanical stimulation of the mucosa. Impaled neurons were injected with dye (Lucifer yellow or biocytin), and their shapes were determined. All neurons were 5-12 mm from the stimulus, a brush stroke that deformed the mucosal villi. Neurons were classified as S-neurons or AH-neurons (Hirst et al., 1974). About 40% of S-neurons oral to a stimulus responded with bursts of fast EPSPs (average frequency, 15-40 Hz); these neurons were in ascending reflex pathways. About 60% of S-neurons anal to a stimulus responded with similar bursts of fast EPSPs or slow depolarizations; these neurons were in descending pathways. Only 2 of 48 AH-neurons responded, both in descending pathways. Most S-neurons in either ascending or descending pathways received inputs from at least 2 or 3 other neurons. Action potentials evoked during a response averaged 3-10 Hz in frequency, with occasional bursts at up to 100 Hz. The speed of conduction along the reflex pathways was about 0.5 m/sec. All S-neurons were uniaxonal, but they differed in size, dendritic morphology, and projections. The axons of S-neurons injected with biocytin were followed up to 7 mm within the myenteric plexus. Three S-neurons projected to the tertiary plexus and were probably longitudinal muscle motor neurons; 2 of these were in descending pathways. Five S-neurons projected along the intestine and had varicose collaterals in some ganglia. These neurons were probably interneurons; 3 were descending and 2 ascending, and all responded in the appropriate reflex pathway. Many S-neurons had short axons that entered the circular muscle and were probably circular muscle motor neurons. Others projected several millimeters along the intestine before entering the circular muscle or fading beyond detection. From this study, we have been able to deduce the circuits mediating ascending and descending mucosa-to-muscle reflexes. It is concluded that AH-neurons are primary sensory neurons and S-neurons are interneurons and muscle motor neurons in the circuits.