Mechanisms underlying distension-evoked peristalsis in guinea pig distal colon: is there a role for enterochromaffin cells?

2011 ◽  
Vol 301 (3) ◽  
pp. G519-G527 ◽  
Author(s):  
Nick J. Spencer ◽  
Sarah J. Nicholas ◽  
Lucy Robinson ◽  
Melinda Kyloh ◽  
Nicholas Flack ◽  
...  
Keyword(s):  
Guinea Pig ◽  
Myenteric Plexus ◽  
Distal Colon ◽  
Solid Content ◽  
Submucosal Plexus ◽  
Fecal Pellets ◽  
Colonic Wall ◽  
Ec Cells ◽  
Colonic Distension ◽  
Muscularis Externa

The mechanisms underlying distension-evoked peristalsis in the colon are incompletely understood. It is well known that, following colonic distension, 5-hydroxytryptamine (5-HT) is released from enterochromaffin (EC) cells in the intestinal mucosa. It is also known that exogenous 5-HT can stimulate peristalsis. These observations have led some investigators to propose that endogenous 5-HT release from EC cells might be involved in the initiation of colonic peristalsis, following distension. However, because no direct evidence exists to support this hypothesis, the aim of this study was to determine directly whether release of 5-HT from EC cells was required for distension-evoked colonic peristalsis. Real-time amperometric recordings of 5-HT release and video imaging of colonic wall movements were performed on isolated segments of guinea pig distal colon, during distension-evoked peristalsis. Amperometric recordings revealed basal and transient release of 5-HT from EC cells before and during the initiation of peristalsis, respectively. However, removal of mucosa (and submucosal plexus) abolished 5-HT release but did not inhibit the initiation of peristalsis nor prevent the propagation of fecal pellets or intraluminal fluid. Maintained colonic distension by fecal pellets induced repetitive peristaltic waves, whose intrinsic frequency was also unaffected by removal of the submucosal plexus and mucosa, although their propagation velocities were slower. In conclusion, the mechanoreceptors and sensory neurons activated by radial distension to initiate peristalsis lie in the myenteric plexus and/or muscularis externa, and their activation does not require the submucosal plexus, release of 5-HT from EC cells, nor the presence of the mucosa. The propagation of peristalsis and propulsion of liquid or solid content along the colon is entrained by activity within the myenteric plexus and/or muscularis externa and does not require sensory feedback from the mucosa, nor neural inputs arising from submucosal ganglia.

Peristalsis and propulsion of colonic content can occur after blockade of major neuroneuronal and neuromuscular transmitters in isolated guinea pig colon

2013 ◽  
Vol 305 (12) ◽  
pp. G933-G939 ◽  
Author(s):  
T. C. Sia ◽  
S. J. Brookes ◽  
P. G. Dinning ◽  
D. A. Wattchow ◽  
N. J. Spencer
Keyword(s):  
Guinea Pig ◽  
Nicotinic Receptors ◽  
Fecal Pellet ◽  
Distal Colon ◽  
Fundamental Question ◽  
Fecal Pellets ◽  
Colonic Wall ◽  
Excitatory Neurotransmitters ◽  
Velocity Of Propagation ◽  
Normal Propagation

We recently identified hexamethonium-resistant peristalsis in the guinea pig colon. We showed that, following acute blockade of nicotinic receptors, peristalsis recovers, leading to normal propagation velocities of fecal pellets along the colon. This raises the fundamental question: what mechanisms underlie hexamethonium-resistant peristalsis? We investigated whether blockade of the major receptors that underlie excitatory neuromuscular transmission is required for hexamethonium-resistant peristalsis. Video imaging of colonic wall movements was used to make spatiotemporal maps and determine the velocity of peristalsis. Propagation of artificial fecal pellets in the guinea pig distal colon was studied in hexamethonium, atropine, ω-conotoxin (GVIA), ibodutant (MEN-15596), and TTX. Hexamethonium and ibodutant alone did not retard peristalsis. In contrast, ω-conotoxin abolished peristalsis in some preparations and reduced the velocity of propagation in all remaining specimens. Peristalsis could still occur in some animals in the presence of hexamethonium + atropine + ibodutant + ω-conotoxin. Peristalsis never occurred in the presence of TTX. The major finding of the current study is the unexpected observation that peristalsis can occur after blockade of the major excitatory neuroneuronal and neuromuscular transmitters. Also, the colon retained an intrinsic polarity in the presence of these antagonists and was only able to expel pellets in an aboral direction. The nature of the mechanism(s)/neurotransmitter(s) that generate(s) peristalsis and facilitate(s) natural fecal pellet propulsion, after blockade of major excitatory neurotransmitters, at the neuroneuronal and neuromuscular junction remains to be identified.

Peristalsis and fecal pellet propulsion do not require nicotinic, purinergic, 5-HT3, or NK3 receptors in isolated guinea pig distal colon

2010 ◽  
Vol 298 (6) ◽  
pp. G952-G961 ◽  
Author(s):  
Sarah Nicholas ◽  
Nick J. Spencer
Keyword(s):  
Guinea Pig ◽  
Propagation Velocity ◽  
Fecal Pellet ◽  
Distal Colon ◽  
Inhibitory Effect ◽  
Propulsive Force ◽  
Fecal Pellets ◽  
Spatiotemporal Mapping ◽  
Direct Contrast ◽  
Mapping Techniques

The neuronal mechanism by which distension of the colon triggers peristalsis and the propulsion of colonic contents is incompletely understood. In this study, we used video imaging and spatiotemporal mapping techniques to investigate the neuroneuronal mechanisms underlying peristalsis in isolated guinea pig distal colon. In direct contrast to previous studies, we found that hexamethonium (100 μM–1 mM) or mecamylamine (20 μM) never abolished peristalsis or fecal pellet propulsion, although a temporary blockade of peristalsis was common, giving the impression perhaps that peristalsis was blocked permanently. During the initiation of peristalsis, the intraluminal propulsive force applied to an inserted fecal pellet was significantly reduced by hexamethonium 100 μM, even though, once initiated, the propagation velocity of fecal pellets was never reduced by nicotinic antagonists. In the presence of hexamethonium or mecamylamine, further addition of PPADS (10 μM), ondansetron (1 μM), and SR 142801 (300 nM) had no inhibitory effect on the propagation velocity of fecal pellets. In these preparations, antagonists for nicotinic, purinergic (P2), serotonergic (5-HT3), or tachykinergic (NK3) receptors always abolished responses to the agonists for these receptors, confirming that when peristalsis occurred, nicotinic, P2, 5-HT3, and NK3 receptors were blocked. Tetrodotoxin abolished nonnicotinic peristalsis. In summary, nicotinic transmission contributes to excitatory neuroneuronal transmission underlying peristalsis and fecal pellet propulsion but is not required for peristalsis, nor fecal pellet propulsion, as once thought. These observations could be explained by an excitatory nonnicotinic neuroneuronal pathway that can generate peristalsis and induce normal fecal pellet propagation velocities but does not require nicotinic, P2, 5-HT3, or NK3 receptors.

Electrophysiological properties of neurons in submucosal ganglia of guinea pig distal colon

1991 ◽  
Vol 260 (6) ◽  
pp. G835-G841 ◽  
Author(s):  
T. Frieling ◽  
H. J. Cooke ◽  
J. D. Wood
Keyword(s):  
Guinea Pig ◽  
Ganglion Cells ◽  
Distal Colon ◽  
Submucosal Plexus ◽  
Electrophysiological Properties ◽  
Small Intestinal ◽  
Type 3

Intracellular recording methods were used in vitro to study the electrophysiological behavior of neurons in ganglia of the submucosal plexus in the distal colon of the guinea pig. The results revealed subpopulations of submucosal ganglion cells that corresponded to the AH/type 2, S/type 1, type 3, and type 4 subpopulations found elsewhere in the intestine. Electrical behavior of colonic submucosal neurons differed from the myenteric plexus of the colon, rectum, and stomach and the small intestinal submucosal plexus mainly in the relative proportions of the different subpopulations. Regional differences in this respect may be a reflection of functional specialization in the diverse regions of the alimentary canal.

Electrical rhythmicity and spread of action potentials in longitudinal muscle of guinea pig distal colon

2002 ◽  
Vol 282 (5) ◽  
pp. G904-G917 ◽  
Author(s):  
Nick J. Spencer ◽  
Grant W. Hennig ◽  
Terence K. Smith
Keyword(s):  
Guinea Pig ◽  
Myenteric Plexus ◽  
Action Potentials ◽  
Longitudinal Muscle ◽  
Circular Muscle ◽  
Intrinsic Property ◽  
Distal Colon ◽  
Separation Distance ◽  
Spontaneous Action ◽  
Cells Of Cajal

Using simultaneous intracellular recordings, we have characterized 1) electrical activity in the longitudinal muscle (LM) of isolated segments of guinea pig distal colon free to contract spontaneously and 2) extent of propagation of spontaneous action potentials around the circumference of the colon. In all animals, rhythmical spontaneous depolarizations (SDs) were recorded that are usually associated with the generation of action potentials. Recordings from pairs of LM cells, separated by 100 μm in the circumferential axis, revealed that each action potential was phase locked at the two electrodes (mean propagation velocity: 3 mm/s). However, at an increased electrode separation distance of 1 mm circumferentially, action potentials and SDs became increasingly uncoordinated at the two recording sites. No SDs or action potentials ever propagated from one circumferential edge to the other (i.e., 13 mm apart). When LM strips were separated from the myenteric plexus and circular muscle, rhythmically firing SDs and action potentials were still recorded. Atropine (1 μM) or tetrodotoxin (1 μM) either reduced the frequency of SDs or temporily abolished activity, whereas nifedipine (1 μM) always abolished SDs and action potentials. Kit-positive interstitial cells of Cajal were present at the level of the myenteric plexus and circular and longitudinal muscle. In summary, SDs and action potentials in LM propagate over discrete localized zones, usually <1 mm around the circumference of the colon. Furthermore, in contrast to the classic slow wave, rhythmic depolarizations in LM appear to be generated by an intrinsic property of the smooth muscle itself and are critically dependent on opening of L-type Ca2+ channels.

Electrical responses of the muscularis externa to distension of the isolated guinea-pig distal colon

2008 ◽  
Vol 4 (3) ◽  
pp. 145-156 ◽  
Author(s):  
T. K. SMITH ◽  
R. A. BYWATER ◽  
G. S. TAYLOR ◽  
M. E. HOLMAN
Keyword(s):  
Guinea Pig ◽  
Distal Colon ◽  
Muscularis Externa ◽  
Electrical Responses

Correlation of morphology, electrophysiology and chemistry of neurons in the myenteric plexus of the guinea-pig distal colon

1999 ◽  
Vol 76 (1) ◽  
pp. 45-61 ◽  
Author(s):  
A.E.G Lomax ◽  
K.A Sharkey ◽  
P.P Bertrand ◽  
A.M Low ◽  
J.C Bornstein ◽  
...  
Keyword(s):  
Guinea Pig ◽  
Myenteric Plexus ◽  
Distal Colon

Platelet-activating factor in the enteric nervous system of the guinea pig small intestine

2006 ◽  
Vol 291 (5) ◽  
pp. G928-G937 ◽  
Author(s):  
Guo-Du Wang ◽  
Xi-Yu Wang ◽  
Hong-Zhen Hu ◽  
Xiu-Cai Fang ◽  
Sumei Liu ◽  
...  
Keyword(s):  
Nervous System ◽  
Guinea Pig ◽  
Enteric Nervous System ◽  
Motor Neurons ◽  
Myenteric Plexus ◽  
Platelet Activating Factor ◽  
Secretory Diarrhea ◽  
Submucosal Plexus ◽  
Neuronal Protein ◽  
Paf Receptor

Platelet-activating factor (PAF) is a proinflammatory mediator that may influence neuronal activity in the enteric nervous system (ENS). Electrophysiology, immunofluorescence, Western blot analysis, and RT-PCR were used to study the action of PAF and the expression of PAF receptor (PAFR) in the ENS. PAFR immunoreactivity (IR) was expressed by 6.9% of the neurons in the myenteric plexus and 14.5% of the neurons in the submucosal plexus in all segments of the guinea pig intestinal tract as determined by double staining with anti-human neuronal protein antibody. PAFR IR was found in 6.1% of the neurons with IR for calbindin, 35.8% of the neurons with IR for neuropeptide Y (NPY), 30.6% of the neurons with IR for choline acetyltransferase (ChAT), and 1.96% of the neurons with IR for vasoactive intestinal peptide (VIP) in the submucosal plexus. PAFR IR was also found in 1.5% of the neurons with IR for calbindin, 51.1% of the neurons with IR for NPY, and 32.9% of the neurons with IR for ChAT in the myenteric plexus. In the submucosal plexus, exposure to PAF (200–600 nM) evoked depolarizing responses (8.2 ± 3.8 mV) in 12.4% of the neurons with S-type electrophysiological behavior and uniaxonal morphology and in 12.5% of the neurons with AH-type electrophysiological behavior and Dogiel II morphology, whereas in the myenteric preparations, depolarizing responses were elicited by a similar concentration of PAF in 9.5% of the neurons with S-type electrophysiological behavior and uniaxonal morphology and in 12.0% of the neurons with AH-type electrophysiological behavior and Dogiel II morphology. The results suggest that subgroups of secreto- and musculomotor neurons in the submucosal and myenteric plexuses express PAFR. Coexpression of PAFR IR with ChAT IR in the myenteric plexus and ChAT IR and VIP IR in the submucosal plexus suggests that PAF, after release in the inflamed bowel, might act to elevate the excitability of submucosal secretomotor and myenteric musculomotor neurons. Enhanced excitability of motor neurons might lead to a state of neurogenic secretory diarrhea.

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