Stretch-activated neuronal pathways to longitudinal and circular muscle in guinea pig distal colon

2003 ◽  
Vol 284 (2) ◽  
pp. G231-G241 ◽  
Author(s):  
Nick J. Spencer ◽  
Grant W. Hennig ◽  
Terence K. Smith

The role of the longitudinal muscle (LM) layer during the peristaltic reflex in the small and large intestine is unclear. In this study, we have made double and quadruple simultaneous intracellular recordings from LM and circular muscle (CM) cells of guinea pig distal colon to correlate the electrical activities in the two different muscle layers during circumferential stretch. Simultaneous recordings from LM and CM cells (<200 μm apart) at the oral region of the colon showed that excitatory junction potentials (EJPs) discharged synchronously in both muscle layers for periods of up to 6 h. Similarly, at the anal region of the colon, inhibitory junction potentials (IJPs) discharged synchronously in the two muscle layers. Quadruple recordings from LM and CM orally at the same time as from the LM and CM anally revealed that IJPs occurred synchronously in the LM and CM anally at the same time as EJPs in LM and CM located 20 mm orally. Oral EJPs and anal IJPs were linearly related in amplitude between the two muscle layers. Spatiotemporal maps generated from simultaneous video imaging of the movements of the colon, combined with intracellular recordings, revealed that some LM contractions orally could be correlated in time with IJPs in CM cells anally. N ω-nitro-l-arginine (l-NA; 100 μM) abolished the IJP in LM, whereas a prominent l-NA-resistant “fast” IJP was always observed in CM. In summary, in stretched preparations, synchronized EJPs in both LM and CM orally are generated by synchronized firing of many ascending interneurons, which simultaneously activate excitatory motor neurons to both muscle layers. Similarly, synchronized IJPs in both LM and CM anally are generated by synchronized firing of many descending interneurons, which simultaneously activate inhibitory motor neurons to both muscle layers. This synchronized motor activity ensures that both muscles around the entire circumference are excited orally at the same time as inhibited anally, thus producing net aboral propulsion.

2001 ◽  
Vol 443 (1) ◽  
pp. 15-26 ◽  
Author(s):  
Hiroyuki Konomi ◽  
Adrian C.B. Meedeniya ◽  
Maria E. Simula ◽  
James Toouli ◽  
Gino T.P. Saccone

1989 ◽  
Vol 256 (3) ◽  
pp. G540-G545 ◽  
Author(s):  
P. Holzer

Isolated segments of the guinea pig small intestine were used to examine the transmitter circuitry of the neural pathways subserving the ascending enteric reflex (AER) contraction of the circular muscle. Inflation of an intraluminal balloon provided the distension stimulus for the AER. The ascending contraction was reduced to 5% of its original amplitude by atropine and to 10% by hexamethonium, which indicates that cholinergic interneurons and cholinergic motor neurons constitute the main AER pathway. However, in the continued presence of atropine or hexamethonium for 60 min, the AER recovered to approximately 30% of its original amplitude. The atropine-resistant AER was blocked by hexamethonium and the tachykinin antagonist spantide [( D-Arg1,D-Trp7,9, Leu11]-substance P) suggesting that it involved cholinergic interneurons and tachykinin-utilizing motor neurons. The hexamethonium-resistant AER was abolished by atropine but left unaffected by spantide, suggesting the participation of as yet unidentified interneurons and cholinergic motor neurons. These findings demonstrate that the AER is mediated by multiple neural pathways with different transmitters and that adaptive interactions between these pathways take place after blockade of one of its neurotransmitters systems.


1984 ◽  
Vol 246 (4) ◽  
pp. G361-G371 ◽  
Author(s):  
K. M. Sanders

Studies were performed to determine the role of endogenous prostaglandins (PG) in regulating mechanical and electrical activities of canine ileal circular muscles. Indomethacin, a prostaglandin synthesis blocker, enhanced the amplitude of spontaneous and acetylcholine-stimulated contractions. The increase in mechanical activity caused by indomethacin was accompanied by decreased release of 6-keto-PGF1 alpha, the spontaneous metabolite of prostacyclin, from the muscle. The electrical mechanisms responsible for the changes in mechanical activity caused by indomethacin were investigated by intracellular measurement of electrical activity. The enhanced contractions due to indomethacin correlated with enhanced electrical slow-wave amplitude and generation of action potentials. After indomethacin treatment muscles were exposed to several exogenous prostaglandins to determine which of these compounds might reverse the mechanical effects of indomethacin. Prostacyclin reversed the effects of indomethacin, and PGE2 reversed some of the effects of indomethacin. Prostacyclin also decreased the amplitude of electrical slow waves and abolished action potentials. These electrical effects were associated with decreased contractile amplitude. It is concluded that the dominant prostaglandin responsible for the "prostaglandin effect" in canine ileal circular muscle must be inhibitory to spontaneous and acetylcholine-stimulated contractions. The mechanical effects attributed to endogenous prostaglandin appear to be due to an electrical mechanism. Based on the evidence presented prostacyclin emerges as the most likely candidate for the role of "dominant" prostaglandin, but PGE2 may also contribute as a modulator of electrical and mechanical activities.


2012 ◽  
Vol 44 ◽  
pp. S127
Author(s):  
B. Balestra ◽  
R. Vicini ◽  
O. Pastoris ◽  
M. Cervio ◽  
V. Stanghellini ◽  
...  
Keyword(s):  

2007 ◽  
Vol 292 (4) ◽  
pp. G1162-G1172 ◽  
Author(s):  
R. M. Gwynne ◽  
J. C. Bornstein

Mechanisms underlying nutrient-induced segmentation within the gut are not well understood. We have shown that decanoic acid and some amino acids induce neurally dependent segmentation in guinea pig small intestine in vitro. This study examined the neural mechanisms underlying segmentation in the circular muscle and whether the timing of segmentation contractions also depends on slow waves. Decanoic acid (1 mM) was infused into the lumen of guinea pig duodenum and jejunum. Video imaging was used to monitor intestinal diameter as a function of both longitudinal position and time. Circular muscle electrical activity was recorded by using suction electrodes. Recordings from sites of segmenting contractions showed they are always associated with excitatory junction potentials leading to action potentials. Recordings from sites oral and anal to segmenting contractions revealed inhibitory junction potentials that were time locked to those contractions. Slow waves were never observed underlying segmenting contractions. In paralyzed preparations, intracellular recording revealed that slow-wave frequency was highly consistent at 19.5 (SD 1.4) cycles per minute (c/min) in duodenum and 16.6 (SD 1.1) c/min in jejunum. By contrast, the frequencies of segmenting contractions varied widely (duodenum: 3.6–28.8 c/min, median 10.8 c/min; jejunum: 3.0–27.0 c/min, median 7.8 c/min) and sometimes exceeded slow-wave frequencies for that region. Thus nutrient-induced segmentation contractions in guinea pig small intestine do not depend on slow-wave activity. Rather they result from a neural circuit producing rhythmic localized activity in excitatory motor neurons, while simultaneously activating surrounding inhibitory motor neurons.


1989 ◽  
Vol 256 (3) ◽  
pp. C466-C477 ◽  
Author(s):  
T. K. Smith ◽  
J. B. Reed ◽  
K. M. Sanders

Pacemaker activity in the canine proximal colon occurs at the submucosal and myenteric borders of the circular layer [Am. J. Physiol. 252 (Cell Physiol. 21): C215-C224 and C290-C299, 1987]. The present study investigated the neural regulation of rhythmic electrical activity. Spontaneous inhibitory junction potentials (IJPs) were observed in intracellular recordings from circular muscle cells near the myenteric border. The amplitudes of these events decayed with distance through the circular layer. Stimulation at the myenteric plexus surface evoked IJPs that mimicked the spontaneous events. Stimulation at the submucosal surface evoked IJPs in adjacent cells that were of shorter duration and of different waveform than myenteric IJPs. Amplitudes of IJPs evoked by stimulation near either surface decayed with distance from the site of stimulation. The decay functions for IJPs were essentially identical to the decay of spontaneous slow waves or myenteric potential oscillations. Spontaneous and evoked IJPs affected the amplitudes, durations, and patterns of ongoing rhythmic electrical activity. The data suggest that myenteric and submucosal pacemaker populations may be innervated by different populations of inhibitory nerve fibers. Innervation appears to be heterogeneous with dense populations of inhibitory nerve fibers predominantly located in the pacemaker regions. Neural regulations of pacemaker activity influences rhythmic electrical activity throughout the muscularis.


1997 ◽  
Vol 329 (1) ◽  
pp. 85-91 ◽  
Author(s):  
Hiroyoshi Kakuyama ◽  
Atsukazu Kuwahara ◽  
Tohru Mochizuki ◽  
Minoru Hoshino ◽  
Noboru Yanaihara

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