scholarly journals Unique Neural Circuit Connectivity of Mouse Proximal, Middle and Distal Colon Defines Regional Colonic Motor Patterns

Author(s):  
Andrea Nestor-Kalinoski ◽  
Kristen M. Smith-Edwards ◽  
Kimberly Meerschaert ◽  
Joseph F. Margiotta ◽  
Bartek Rajwa ◽  
...  
2007 ◽  
Vol 292 (1) ◽  
pp. G419-G428 ◽  
Author(s):  
L. Wang ◽  
V. Martínez ◽  
H. Kimura ◽  
Y. Taché

Serotonin [5-hydroxytryptamine (5-HT)] acts as a modulator of colonic motility and secretion. We characterized the action of the 5-HT precursor 5-hydroxytryptophan (5-HTP) on colonic myenteric neurons and propulsive motor activity in conscious mice. Fos immunoreactivity (IR), used as a marker of neuronal activation, was monitored in longitudinal muscle/myenteric plexus whole mount preparations of the distal colon 90 min after an intraperitoneal injection of 5-HTP. Double staining of Fos IR with peripheral choline acetyltransferase (pChAT) IR or NADPH-diaphorase activity was performed. The injection of 5-HTP (0.5, 1, 5, or 10 mg/kg ip) increased fecal pellet output and fluid content in a dose-related manner, with a peak response observed within the first 15 min postinjection. 5-HTP (0.5–10 mg/kg) dose dependently increased Fos expression in myenteric neurons, with a maximal response of 9.9 ± 1.0 cells/ganglion [ P < 0.05 vs. vehicle-treated mice (2.3 ± 0.6 cells/ganglion)]. There was a positive correlation between Fos expression and fecal output. Of Fos-positive ganglionic cells, 40 ± 4% were also pChAT positive and 21 ± 5% were NADPH-diaphorase positive in response to 5-HTP, respectively. 5-HTP-induced defecation and Fos expression were completely prevented by pretreatment with the selective 5-HT4 antagonist RS-39604. These results show that 5-HTP injected peripherally increases Fos expression in different populations of cholinergic and nitrergic myenteric neurons in the distal colon and stimulates propulsive colonic motor function through 5-HT4 receptors in conscious mice. These findings suggest an important role of activation of colonic myenteric neurons in the 5-HT4 receptor-mediated colonic propulsive motor response.


2016 ◽  
Vol 310 (3) ◽  
pp. G181-G192 ◽  
Author(s):  
Ji-Hong Chen ◽  
Zixian Yang ◽  
Yuanjie Yu ◽  
Jan D. Huizinga

The rabbit proximal colon is similar in structure to the human colon. Our objective was to study interactions of different rhythmic motor patterns focusing on haustral boundary contractions, which create the haustra, using spatiotemporal mapping of video recordings. Haustral boundary contractions were seen as highly rhythmic circumferential ring contractions that propagated slowly across the proximal colon, preferentially but not exclusively in the anal direction, at ∼0.5 cycles per minute; they were abolished by nerve conduction blockers. When multiple haustral boundary contractions propagated in the opposite direction, they annihilated each other upon encounter. Ripples, myogenic propagating ring contractions at ∼9 cycles per min, induced folding and unfolding of haustral muscle folds, creating an anarchic appearance of contractile activity, with different patterns in the three intertaenial regions. Two features of ripple activity were prominent: frequent changes in propagation direction and the occurrence of dislocations showing a frequency gradient with the highest intrinsic frequency in the distal colon. The haustral boundary contractions showed an on/off/on/off pattern at the ripple frequency, and the contraction amplitude at any point of the colon showed waxing and waning. The haustral boundary contractions are therefore shaped by interaction of two pacemaker activities hypothesized to occur through phase-amplitude coupling of pacemaker activities from interstitial cells of Cajal of the myenteric plexus and of the submuscular plexus. Video evidence shows the unique role haustral folds play in shaping contractile activity within the haustra. Muscarinic agents not only enhance the force of contraction, they can eliminate one and at the same time induce another neurally dependent motor pattern.


2001 ◽  
Vol 280 (5) ◽  
pp. R1371-R1381 ◽  
Author(s):  
Hans-Rudolf Berthoud ◽  
Penny A. Lynn ◽  
L. Ashley Blackshaw

Mechano- and chemosensitive extrinsic primary afferents innervating the gastrointestinal tract convey important information regarding the state of ingested nutrients and specific motor patterns to the central nervous system via splanchnic and vagal nerves. Little is known about the organization of peripheral receptive sites of afferents and their correspondence to morphologically identified terminal structures. Mechano- and chemosensory characteristics and receptive fields of single vagal fibers innervating the stomach as well as lumbar splanchnic nerves innervating the distal colon were identified using an in vitro perifusion system. Twenty-three (17%) of one-hundred thirty-six vagal units identified were found to have multiple, punctate receptive fields, up to 35 mm apart, and were distributed throughout the stomach. Evidence was based on similarity of generated spike forms, occlusion, and latency determinations. Most responded with brief bursts of activity to mucosal stroking with von Frey hairs (10–200 mg) but not to stretch, and 32% responded to capsaicin (10−5M). They were classified as rapidly adapting mucosal receptors. Four (8%) of fifty-three single units recorded from the lumbar splanchnic nerve had more than one, punctate receptive field in the distal colon, up to 40 mm apart. They responded to blunt probing, particularly from the serosal side, and variously to chemical stimulation with 5-hydroxytryptamine and capsaicin. We conclude that a proportion of gastrointestinal mechanosensors has multiple receptive fields and suggest that they integrate mechanical and chemical information from an entire organ, constituting the generalists in visceral sensation.


1991 ◽  
Vol 260 (4) ◽  
pp. G646-G652 ◽  
Author(s):  
M. Dapoigny ◽  
S. K. Sarna

We investigated the effect of physical exercise on colonic motor activity in the fasted and fed states in six conscious dogs. Each dog was implanted with nine strain gauge transducers: three on the proximal, three on the middle, and three on the distal colon. The dogs ran for 1 h on a treadmill at 5 km/h (slope 5%). In the fasted state, the dogs exercised during the 5th h of recording after an overnight fast, and in the fed state during the 1st, 3rd, and 5th postprandial hour. In the fasted state, exercise significantly decreased the frequency of colonic migrating motor complexes (MMCs) but had no effect on the total or the mean duration of contractile states in the proximal, middle, and distal colon. Postprandially, exercise disrupted colonic MMCs and replaced them with nonmigrating motor complexes in all three periods of exercise (1st, 3rd, and 6th h). Exercise also increased the total duration per hour of contractile activity throughout the colon during the 1st and 3rd h and only in the distal colon during the 6th h after the meal. The dogs never defecated during rest in the fasted or the fed state. Shortly after the start of exercise in the fasted and fed states, giant migrating contractions (GMCs) occurred, and they were followed by defecation. In approximately 40% of the experiments, another GMC originated in the proximal colon, approximately 10 min after the first defecation, and migrated caudad up to the middle colon. These GMCs were not associated with defecation but caused mass movements.(ABSTRACT TRUNCATED AT 250 WORDS)


1994 ◽  
Vol 107 (5) ◽  
pp. 1372-1381 ◽  
Author(s):  
Yoshiyuki Furukawa ◽  
Ian J. Cook ◽  
Voula Panagopoulos ◽  
R. Douglas McEvoy ◽  
David J. Sharp ◽  
...  

2016 ◽  
Vol 150 (4) ◽  
pp. S537
Author(s):  
Marcello Costa ◽  
Lukasz Wiklendt ◽  
Nick J. Spencer ◽  
Simon J. Brookes ◽  
Philip Dinning

Author(s):  
Aaron P. Cook ◽  
Michael P. Nusbaum

Studies elucidating modulation of microcircuit activity in isolated nervous systems have revealed numerous insights regarding neural circuit flexibility, but this approach limits the link between experimental results and behavioral context. To bridge this gap, we studied feeding behavior-linked modulation of microcircuit activity in the isolated stomatogastric nervous system (STNS) of male Cancer borealis crabs. Specifically, we removed hemolymph from a crab that was unfed for ≥24 h ('unfed' hemolymph) or fed 15 min - 2 h before hemolymph removal ('fed' hemolymph). After feeding, the first significant foregut emptying occurred >1 h later and complete emptying required ≥6 h. We applied the unfed or fed hemolymph to the stomatogastric ganglion (STG) in an isolated STNS preparation from a separate, unfed crab to determine its influence on the VCN (ventral cardiac neuron)-triggered gastric mill (chewing)- and pyloric (filtering of chewed food) rhythms. Unfed hemolymph had little influence on these rhythms, but fed hemolymph from each examined time-point (15 min, 1- or 2 h post-feeding) slowed one or both rhythms without weakening circuit neuron activity. There were also distinct parameter changes associated with each time-point. One change unique to the 1 h time-point (i.e. reduced activity of one circuit neuron during the transition from the gastric mill retraction to protraction phase) suggested the fed hemolymph also enhanced the influence of a projection neuron which innervates the STG from a ganglion isolated from the applied hemolymph. Hemolymph thus provides a feeding state-dependent modulation of the two feeding-related motor patterns in the C. borealis STG.


2019 ◽  
Vol 316 (1) ◽  
pp. G32-G44 ◽  
Author(s):  
Marcello Costa ◽  
Lauren J. Keightley ◽  
Lukasz Wiklendt ◽  
Timothy J. Hibberd ◽  
John W. Arkwright ◽  
...  

In the guinea pig distal colon, nonpropulsive neurally mediated motor patterns have been observed in different experimental conditions. Isolated segments of guinea pig distal colon were used to investigate these neural mechanisms by simultaneously recording wall motion, intraluminal pressure, and smooth muscle electrical activity in different conditions of constant distension and in response to pharmacological agents. Three distinct neurally dependent motor patterns were identified: transient neural events (TNEs), cyclic motor complexes (CMC), and distal colon migrating motor complexes (DCMMC). These could occur simultaneously and were distinguished by their electrophysiological, mechanical, and pharmacological features. TNEs occurred at irregular intervals of ~3s, with bursts of action potentials at 9 Hz. They propagated orally at 12 cm/s via assemblies of ascending cholinergic interneurons that activated final excitatory and inhibitory motor neurons, apparently without involvement of stretch-sensitive intrinsic primary afferent neurons. CMCs occurred during maintained distension and consisted of clusters of closely spaced TNEs, which fused to cause high-frequency action potential firing at 7 Hz lasting ~10 s. They generated periodic pressure peaks mediated by stretch-sensitive intrinsic primary afferent neurons and by cholinergic interneurons. DCMMCs were generated by ongoing activity in excitatory motor neurons without apparent involvement of stretch-sensitive neurons, cholinergic interneurons, or inhibitory motor neurons. In conclusion, we have identified three distinct motor patterns that can occur concurrently in the isolated guinea pig distal colon. The mechanisms underlying the generation of these neural patterns likely involve recruitment of different populations of enteric neurons with distinct temporal activation properties.


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