Neurotensin Changes Propulsive Activity into a Segmental Motor Pattern in the Rat Colon

Abstract

Background/AimsNeurotensin is a gut-brain peptide with both inhibitory and excitatory actions on the colonic musculature; our objective was to understand the implications of this for motor patterns occurring in the intact colon of the rat. MethodsThe effects of neurotensin with concentrations ranging from 0.1-100 nM were studied in the intact rat colon in vitro, by investigating spatio-temporal maps created from video recordings of colonic motility before and after neurotensin. ResultsLow concentration of neurotensin (0.1-1 nM) inhibited propagating long distance contractions and rhythmic propagating motor complexes; in its place a slow propagating rhythmic segmental motor pattern developed. The neurotensin receptor 1 antagonist SR-48692 prevented the development of the segmental motor pattern. Higher concentrations of neurotensin (10 nM and 100 nM) were capable of restoring long distance contraction activity and inhibiting the segmental activity. The slow propagating segmental contraction showed a rhythmic contraction --relaxation cycle at the slow wave frequency originating from the interstitial cells of Cajal associated with the myenteric plexus pacemaker. High concentrations given without prior additions of low concentrations did not evoke the segmental motor pattern. These actions occurred when neurotensin was given in the bath solution or intraluminally. The segmental motor pattern evoked by neurotensin was inhibited by the neural conduction blocker lidocaine. ConclusionsNeurotensin (0.1-1 nM) inhibits the dominant propulsive motor patterns of the colon and a distinct motor pattern of rhythmic slow propagating segmental contractions develops. This motor pattern has the hallmarks of haustral boundary contractions. (J Neurogastroenterol Motil 2016;22:517-528)

Relationships Between Distention-, Butyrate- and Pellet-Induced Stimulation of Peristalsis in the Mouse Colon

“…In addition to these two motor patterns, there are three other motor patterns in the mouse colon, previously characterized in the rat colon: myogenic ripples (Chen et al, 2013), proximal rhythmic contractions (Li et al, 2016) and distal rhythmic propagating motor complexes (Chen et al, 2013;Li et al, 2016). Here we see many LDCs we have previously identified as "broken LDCs" (Chen et al, 2013), where it appears that the LDC is interrupted by one or many streaks of inhibition.…”

“…We recently demonstrated in the rabbit colon that the characteristics of this motor complex are dramatically different at different levels of excitation (Shokrollahi et al, 2019). In the rabbit, mouse and rat, we and others have identified the long distance contraction (LDC) as the most forceful circumferential propulsive contraction evoked by distention that propels content down the colon; it is the most forceful expression of the CMC (Chen et al, 2013;Kendig and Grider, 2015;Yu et al, 2015;Li et al, 2016;Vincent et al, 2018). The propulsive nature of the LDC can be measured by its association with 3-5 ml outflow .…”

Intraluminal prucalopride increases propulsive motor activities via luminal 5‐HT4 receptors in the rabbit colon

“…In the rabbit, mouse, and rat, we and others have identified the LDC as the most forceful circumferential propulsive contraction evoked by distention that propels content down the colon . The propulsive nature of LDCs can be measured by their association with 3‐5 mL outflow .…”

“…In the rabbit, mouse, and rat, we and others have identified the LDC as the most forceful circumferential propulsive contraction evoked by distention that propels content down the colon. 5,22,[36][37][38] The propulsive nature of LDCs can be measured by their association with 3-5 mL outflow. 39 LDCs have a characteristic triangular shape in spatiotemporal maps, due to the fact that the most proximal part of the colon remains contracted while the front of the contraction propagates anally, preceded by relaxation.…”

Colonic Transit Time and Gut Peptides in Adult Patients with Slow and Normal Colonic Transit Constipation

“…A study on the motor patterns occurring in the rat intact colon put in evidence that low neurotensin concentrations inhibit the propagating long distance contractions and rhythmic propagating motor complexes; in its place a slow propagating rhythmic segmental motor pattern occurs. Moreover, high concentrations of neurotensin are capable of restoring long distance contraction activity and inhibiting the segmental activity [ 37 ]. If confirmed in humans, this behaviour of neurotensin could explain the physiological background of colonic slow transit time in some patients with constipation.…”