The role of tension receptors in colonic mechanosensitivity in humans

Abstract

Background: Perception of colonic distension, which is enhanced in a subset of patients with irritable bowel syndrome, requires activation of mechanoreceptors. In animal studies, distension activates both in series ("tension") and in parallel ("elongation") mechanoreceptors. During active contractions against a fixed volume balloon, tension receptors are activated without elongation of receptor activation.

Aim: To evaluate the role of tension receptors in the perception of mechanical stimuli from the colon in healthy subjects.

Methods: A 700 ml balloon connected to a barostat-manometer assembly was placed in the descending colon of 10 healthy subjects. After volume controlled distension (50 ml/2 minutes) to assess the first perception threshold, fixed volume subthreshold distension (122 (16) ml) was maintained for a 30 minute period before and after administration of neostigmine 0.5 mg intravenously. Mean intraballoon pressure, number, amplitude, and duration of contractions, and frequency of sensations were analysed. The period after neostigmine was divided into 10 second intervals and evaluated for the occurrence of contractions and onset of sensations. Fisher's exact test was applied to calculate the sensation-contraction association probability (SAP) as (1.0-p)x100%.

Results: Neostigmine increased intraballoon pressure (p<0.01), number of contractions (p<0.01), and number of sensations (p<0.01) per minute in all subjects. In seven of 10 subjects a significant association (SAP >95%) was found between sensations and contractions. In the remaining subjects, contractions were not associated with sensations and had lower amplitude (p<0.05) and duration (p<0.01) compared with contractions in the other seven subjects.

Conclusion: In humans, tension receptors are involved in mediating colonic mechanosensitivity.

Figure 1

Schematic representation of the response of tension and elongation receptors.

Figure 2

(A) Scheme of the experimental procedure performed in each subject. (B) Example of part of a tracing recorded by the barostat in one subject after administration of neostigmine. The vertical axis shows intraballoon pressure recorded by the barostat. Each marker indicates the onset of sensation. The number identifies the intensity of sensation chosen by the subject. Note the temporal relation between contractions and sensations.

Figure 3

(A) Contingency table reporting the mean (SEM) number of intervals with the four combinations of events in subjects with a significant association between contractions and sensation (n = 7). Numbers in parentheses are line percentages. (B) Contingency table reporting the mean (SEM) number of intervals with the four combinations of events in subjects without a significant association between contractions and sensation (n = 3). Numbers in parentheses are line percentages.

Figure 4

Percentage of perceived and unperceived contractions according to different ranges in amplitude.

Figure 5

Relation between amplitude of total contractions and percentage of perceived contractions in each subject.

Figure 6

Example of part of a tracing in one subject after administration of neostigmine. The vertical axis indicates the pressure inside the balloon (channel 1) and the pressure recorded by the manometer at the level of the three side ports below the balloon (channels 6–8). The black arrow indicates a perceived contraction while the white arrows show two unperceived contractions. The marker shows the onset of a sensation. Note that the first unperceived contraction (channel 1) was followed by a high amplitude propagated contraction (HAPC) in the three distal channels (channels 6–8); the second unperceived contraction (channel 1) was not propagated; and the third contraction (channel 1) was perceived (followed in 10 second interval periods by a sensation) and was followed by a HAPC (channels 6–8).