Receptive properties of sacral primary afferent neurons supplying the colon

1. Conscious perception of noxious and innocuous distension of the colon as well as the reflex control of anal continence and defecation largely depend on an intact sacral primary afferent innervation. Here we have studied the functional properties of these visceral primary afferent neurons in the dorsal root S2 in 17 cats. Single fibers projecting into the pelvic nerve were identified electrically and studied with innocuous and noxious mechanical stimulation of colon and anal canal. 2. A total of 59 units responding to one of these stimuli were investigated and they could be separated into two subpopulations of afferents. Thirty-six fibers were reproducibly excited by distension of the colon, but not by mechanical stimulation of the anal canal. They were thin myelinated or unmyelinated fibers with a median conduction velocity of 3.2 m/s. The remaining 23 units had receptive fields in the mucosa of the anal canal and responded readily to an innocuous proximodistal shearing stimulus, but not to distension stimuli applied to the same area. All, but two of these afferents were thin myelinated with a median conduction velocity of 7.7 m/s, which was significantly different from the conduction velocity of afferent neurons responding to distension of the colon. 3. Units responding to distension of the colon had thresholds in the innocuous range of the intracolonic pressure. Receptors that were activated only by noxious intraluminal pressure were absent. On the basis of their response to supramaximal isotonic distension, colonic afferents could be subclassified as phasic (n = 17) or tonic (n = 19) units. Phasic afferents were only transiently excited during filling or emptying of the colon, whereas tonic afferents discharged throughout the distension. The two populations had also significantly different median conduction velocities of 8.0 (n = 16) and 1.7 (n = 15) m/s, respectively. 4. Stimulation response functions were evaluated for 12 tonic afferents. All units encoded an increase of intracolonic pressure by the intensity of their discharge frequency. Increases of intracolonic pressure produced significantly higher discharge frequencies from unmyelinated than from thin myelinated afferents. 5. In three animals the percentage of unmyelinated fibers responding to mechanical stimulation of colon and anal canal was determined. Out of 213 electrically identified unmyelinated units projecting into the pelvic nerve, only 11 (5.2%) were excited. Thus, acute innocuous and noxious mechanical stimuli of the large intestine do not appear to be the adequate stimulus for the large majority of unmyelinated pelvic afferents. 6. In conclusion, distension of the colon and mechanical stimulation of the anal canal activates distinct populations of primary afferent neurons.(ABSTRACT TRUNCATED AT 400 WORDS)