Pelvic afferent reflex control of rectal motility and lumbar colonic efferent discharge mediated by the pontine sympatho-inhibitory region in guinea pigs

Abstract

Rectal motility and the efferent discharge of lumbar colonic nerves (LCED) have previously been shown to be affected by reflex activity activated by rectal stimulation. The sensory limb of this reflex is represented by afferent fibers in pelvic nerves. The present study revealed that this reflex is modulated by supraspinal sympatho-inhibitory regions. Pelvic afferent stimulation led to rectal contraction through the withdrawal of a tonic inhibitory influence of lumbar colonic nerves. The supraspinal region responsible for this antagonism of the rectal-inhibitory colonic nerve activity was localized to the pons. Neither the intravenous administration of atropine nor that of guanethidine (and Eisai compound 865-123, another adrenergic neuron blocking agent) effected the ability of pelvic afferent stimulation to inhibit tonic discharge of lumbar colonic efferent nerves; nevertheless, both agents eliminated the mechanical response of the rectum to stimulation of pelvic afferents. These observations suggest that lumbar sympathetic nerves may tonically inhibit the release of acetylcholine from excitatory neurons in the rectal myenteric plexus. We conclude that descending fibers from the pons are activated as a result of pelvic afferent nerve stimulation. These descending pontine fibers in turn inhibit the firing of sympathetic lumbar colonic nerves. Removal of this tonic restraint leads to rectal contraction.

Integrative control of rectoanal reflex in guinea pigs through lumbar colonic nerves

“…The rectoanal reflex causing both rectal contractions and IAS relaxations were doubly enhanced after LCNs (not HGNs), indicating that the lumbar outflow through the LCNs halved the rectoanal reflex in the guinea pig. This finding is novel and somewhat different from that in our previous reports (22)(23)(24). It seems likely that the inhibition from the pons to lumbar nerve efferent activity was less potent in the present study than in our previous studies (22)(23)(24).…”

“…This finding is novel and somewhat different from that in our previous reports (22)(23)(24). It seems likely that the inhibition from the pons to lumbar nerve efferent activity was less potent in the present study than in our previous studies (22)(23)(24). The difference between our previous result and the present one may involve the different methods of rectal distension that were employed (prompt distension vs. gradual, sustained distension) as discussed below.…”

“…Gradual, sustained rectal distension, as used in the current study, simulating the rectal distension by transported and then reserved two pieces of feces was a more physiological stimulus than those in our previous studies (22)(23)(24), in which prompt, sustained rectal distension was used. In the present study, we were able to induce constant rectal contractions and simultaneous IAS relaxations by means of the rectal distension, although the possibility that the rectal contraction evoked by rectal distension secondarily causes IAS relaxation cannot be excluded.…”

“…The afferent and efferent limbs of the extrinsic excitatory reflex travel in the pelvic nerves, whereas the limbs of the extrinsic inhibitory reflex pass in the lumbar colonic nerves (LCNs) (22). Furthermore, we have found that the inhibitory reflex is suppressed by descending input from the pontine defecation center, leading to a disinhibition of the sacral excitatory reflex and intrinsic excitatory reflex (22)(23)(24). In view of these findings, we have proposed that the lumbar colonic inhibitory reflex contributes to the rectorectal reflex, one important component of the defecation reflex (22-25).…”

“…Furthermore, we have found that the inhibitory reflex is suppressed by descending input from the pontine defecation center, leading to a disinhibition of the sacral excitatory reflex and intrinsic excitatory reflex (22)(23)(24). In view of these findings, we have proposed that the lumbar colonic inhibitory reflex contributes to the rectorectal reflex, one important component of the defecation reflex (22)(23)(24)(25).…”