Modular Nerve Circuit-Mediated Motor Activity in Circular Axis of Rectum in Rat Model (original) (raw)
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Modular and functionally-different descending recto-anal motor pathways in a rat model
Central European Journal of Biology, 2011
We evaluated the motor responses in recto-anal preparations obtained from rats, in terms of the excitation displayed by modules of nerve networks and descending distally directed pathways, when subjected to the mechanographic on-line technique, a partitioned organ bath, electrical stimulation (EFS, 0.8 ms, 5 Hz) and distension. EFS elicited modular contractions, which increased in amplitude distally, in circular muscle rings isolated from the proximal, middle or distal rectum. The modular responses of the internal anal sphincter or anal canal were relaxation or contraction, respectively. The application of EFS to the distal rectum induced a descending contractile response in the anal canal (5.24±0.34 mN), while distension by balloon evoked a descending response consisting of contraction (1.72±0.20 mN) followed by relaxation (3.42±0.24 mN). The responses were sensitive to tetrodotoxin. Atropine considerably depressed the contractions in all preparations. Whether or not atropine was p...
AJP: Gastrointestinal and Liver Physiology, 2012
The functional role of the different classes of visceral afferents that innervate the large intestine is poorly understood. Recent evidence suggests that low-threshold, wide-dynamic-range rectal afferents play an important role in the detection and transmission of visceral pain induced by noxious colorectal distension in mice. However, it is not clear which classes of spinal afferents are activated during naturally occurring colonic motor patterns or during intense contractions of the gut smooth muscle. We developed an in vitro colorectum preparation to test how the major classes of rectal afferents are activated during spontaneous colonic migrating motor complex (CMMC) or pharmacologically induced contraction. During CMMCs, circular muscle contractions increased firing in low-threshold, wide-dynamic-range muscular afferents and muscular-mucosal afferents, which generated a mean firing rate of 1.53 ± 0.23 Hz ( n = 8) under isotonic conditions and 2.52 ± 0.36 Hz ( n = 17) under isome...
Naunyn-schmiedebergs Archives of Pharmacology, 1990
(1) Circularly-oriented muscle strips from the human ileum responded to electrical field stimulation (1–50 Hz) with frequency-related primary relaxation at low frequency and primary contractions at high frequencies of stimulation. Both responses were abolished or markedly reduced by tetrodotoxin (1 μM). (2) Atropine (3 μ M) or omega conotoxin (0.1 μM) reduced but dit not abolish contraction to electrical field stimulation and enhanced the relaxation. Omega conotoxin (0.1 μM) did not affect carbachol-induced contraction nor isoprenaline-induced relaxation. (3) Neurokinin A and substance P (1 nM-1 μM) produced a concentration-dependent contraction. The NK-1 receptor selective agonist, [Pro9]SP sulfone and the NK-2 receptor selective agonist [βAla8]NKA(4-10) prodneed a contraction superimposable to that of substance P and neurokinin A, respectively. On the other hand, [MePhe7]-neurokinin B, an NK-3 receptor selective agonist was ineffective up to 1 [M. The response to substance P or neurokinin A was unaffected by atropine (3 μM). (4) Galanin, up to 0.1 μM produced a weak and inconsistent contraction. (5) Vasoactive intestinal polypeptide (10 nM - 1 μM) produced a concentration-dependent relaxation while human alpha calcitonin gene-related peptide exerted a weak and inconsistent relaxant effect. (6) These findings indicate that both cholinergic excitatory and non-cholinergic inhibitory nerves affect the motility of the circular muscle of the human small intestine. Transmitter release from excitatory nerves seems largely mediated by activation of omega conotoxin-sensitive (N-type) calcium channels. Tachykinins exert a potent contractile effect independently of cholinergic nerves via NK-1 and NK-2 receptors.
Mechanical activation of rectal intraganglionic laminar endings in the guinea pig distal gut
Journal of Physiology-london, 2005
The rectum receives specialized extrinsic afferent innervation by stretch-sensitive, low threshold, slowly adapting mechanoreceptors, with transduction sites shown to correspond to rectal intraganglionic laminar endings (IGLEs). Rectal IGLEs are located in myenteric ganglia, surrounded by the longitudinal and circular smooth muscle layers; in this study we investigated the mechanical stimuli to which they respond. Mechanoreceptors had graded responses to highly focal transmural compression with von Frey hairs. They were activated when stretched circumferentially by imposed increases of both length and load. Under both conditions, firing typically occurred in bursts associated with phasic muscle contractions. However, many contractions did not evoke firing. Longitudinal stretch also evoked firing, again associated with contractile activity. Thus, mechanoreceptors did not show directional sensitivity. Two agonists that excited smooth muscle directly (0.1 µM [β-Ala 8 ]-neurokinin A (4-10) and 1 µM carbachol) activated rectal mechanoreceptors, but not in the presence of Ca 2+ -free solution or when preparations were kept entirely slack. We measured the dimensions, in both longitudinal and circumferential axes, of receptive fields during smooth muscle contractile activity, using video micrography. Contractile activity within the receptive field often differed significantly from the behaviour of the preparation as a whole, providing an explanation for many of the discrepancies between gross contractility and firing. Simultaneous contraction of both muscle layers within the receptive field was the strongest predictor of mechanoreceptor activation. Our results suggest that rectal mechanoreceptors do not act simply as tension receptors: rather they appear to detect mechanical deformation of myenteric ganglia -especially flattening -associated with stretch of the receptive field, or contractions of smooth muscle within the receptive field.
Electrical correlate of circumferential contractions in human colonic circular muscle
Gut, 1988
The role of myogenic electrical activity in the coordination of circumferential contraction of the human colon circular muscle was investigated. Five suction electrodes were placed (5-7 mm apart) on isolated rings of human colon and simultaneously electrical and motor activities were measured. In normal Krebs solution, the slow waves were not synchronised in most preparations studied. The electrical activities at the different recording sites were different with respect to slow wave frequency and amplitude, and amount of spiking activity. This resulted in irregular contractile activity. Cholinergic stimulation resulted in the development of a specific pattern of electrical activity: periodic slow wave activity with superimposed spiking activity which was synchronised over the length of the segment studied. This synchronised electrical activity resulted in regular phasic contractions at the frequency of the bursts of electrical activity (-1/min). The response to carbachol was mediated by muscarinic receptors since it was blocked by atropine. The periodic activity in the continuous presence of carbachol was not the result of periodic input of neural activity as it occurred in the presence of TTX. Intrinsic properties of the muscle cells were responsible for the carbachol induced pattern of activity. The present study presents evidence that the electrical correlate of circumferential contractions is different in man compared with the most commonly studied animal models. It is a specific, stimulus induced pattern of myogenic activity. Its characteristics closely resemble those of a particular pattern of in vivo recorded activity referred to as the 'long spike bursts'.
Neurogenic and myogenic motor activity in the colon of the guinea pig, mouse, rabbit, and rat
AJP: Gastrointestinal and Liver Physiology, 2013
Gastrointestinal motility involves interactions between myogenic and neurogenic processes intrinsic to the gut wall. We have compared the presence of propagating myogenic contractions of the isolated colon in four experimental animals (guinea pig, mouse, rabbit, and rat), following blockade of enteric neural activity. Isolated colonic preparations were distended with fluid, with the anal end either closed or open. Spatiotemporal maps of changes in diameter were constructed from video recordings. Distension-induced peristaltic contractions were abolished by tetrodotoxin (TTX; 0.6 μM) in all animal species. Subsequent addition of carbachol (0.1–1 μM) did not evoke myogenic motor patterns in the mouse or guinea pig, although some activity was observed in rabbit and rat colon. These myogenic contractions propagated both orally and anally and differed from neurogenic propagating contractions in their frequency, extent of propagation, and polarity. Niflumic acid (300 μM), used to block my...
Neurogenic and myogenic motor patterns of rabbit proximal, mid, and distal colon
AJP: Gastrointestinal and Liver Physiology, 2012
The rabbit colon consists of four distinct regions. The motility of each region is controlled by myogenic and neurogenic mechanisms. Associating these mechanisms with specific motor patterns throughout all regions of the colon has not previously been achieved. Three sections of the colon (the proximal, mid, and distal colon) were removed from euthanized rabbits. The proximal colon consists of a triply teniated region and a single tenia region. Spatio-temporal maps were constructed from video recordings of colonic wall diameter, with associated intraluminal pressure recorded from the aboral end. Hexamethonium (100 μM) and tetrodotoxin (TTX; 0.6 μM) were used to inhibit neural activity. Four distinct patterns of motility were detected: 1 myogenic and 3 neurogenic. The myogenic activity consisted of circular muscle (CM) contractions (ripples) that occurred throughout the colon and propagated in both antegrade (anal) and retrograde (oral) directions. The neural activity of the proximal ...
British Journal of Pharmacology, 2008
Background and purpose:To characterize the in vitro motor patterns and the neurotransmitters released by enteric motor neurons (EMNs) in the human sigmoid colon.To characterize the in vitro motor patterns and the neurotransmitters released by enteric motor neurons (EMNs) in the human sigmoid colon.Experimental approach:Sigmoid circular strips were studied in organ baths. EMNs were stimulated by electrical field stimulation (EFS) and through nicotinic ACh receptors.Sigmoid circular strips were studied in organ baths. EMNs were stimulated by electrical field stimulation (EFS) and through nicotinic ACh receptors.Key results:Strips developed weak spontaneous rhythmic contractions (3.67±0.49 g, 2.54±0.15 min) unaffected by the neurotoxin tetrodotoxin (TTX; 1 μM). EFS induced strong contractions during (on, 56%) or after electrical stimulus (off, 44%), both abolished by TTX. Nicotine (1–100 μM) inhibited spontaneous contractions. Latency of off-contractions and nicotine responses were reduced by NG-nitro-L-arginine (1 mM) and blocked after further addition of apamin (1 μM) or the P2Y1 receptor antagonist MRS 2179 (10 μM) and were unaffected by the P2X antagonist NF279 (10 μM) or α-chymotrypsin (10 U mL−1). Amplitude of on- and off-contractions was reduced by atropine (1 μM) and the selective NK2 receptor antagonist Bz-Ala-Ala-D-Trp-Phe-D-Pro-Pro-Nle-NH2 (1 μM). MRS 2179 reduced the amplitude of EFS on- and off-contractions without altering direct muscular contractions induced by ACh (1 nM–1 mM) or substance P (1 nM–10 μM).Strips developed weak spontaneous rhythmic contractions (3.67±0.49 g, 2.54±0.15 min) unaffected by the neurotoxin tetrodotoxin (TTX; 1 μM). EFS induced strong contractions during (on, 56%) or after electrical stimulus (off, 44%), both abolished by TTX. Nicotine (1–100 μM) inhibited spontaneous contractions. Latency of off-contractions and nicotine responses were reduced by NG-nitro-L-arginine (1 mM) and blocked after further addition of apamin (1 μM) or the P2Y1 receptor antagonist MRS 2179 (10 μM) and were unaffected by the P2X antagonist NF279 (10 μM) or α-chymotrypsin (10 U mL−1). Amplitude of on- and off-contractions was reduced by atropine (1 μM) and the selective NK2 receptor antagonist Bz-Ala-Ala-D-Trp-Phe-D-Pro-Pro-Nle-NH2 (1 μM). MRS 2179 reduced the amplitude of EFS on- and off-contractions without altering direct muscular contractions induced by ACh (1 nM–1 mM) or substance P (1 nM–10 μM).Conclusions and implications:Latency of EFS-induced off-contractions and inhibition of spontaneous motility by nicotine are caused by stimulation of inhibitory EMNs coreleasing NO and a purine acting at muscular P2Y1 receptors through apamin-sensitive K+ channels. EFS-induced on- and off-contractions are caused by stimulation of excitatory EMNs coreleasing ACh and tachykinins acting on muscular muscarinic and NK2 receptors. Prejunctional P2Y1 receptors might modulate the activity of excitatory EMNs. P2Y1 and NK2 receptors might be therapeutic targets for colonic motor disorders.British Journal of Pharmacology (2008) 155, 1043–1055; doi:10.1038/bjp.2008.332; published online 1 September 2008Latency of EFS-induced off-contractions and inhibition of spontaneous motility by nicotine are caused by stimulation of inhibitory EMNs coreleasing NO and a purine acting at muscular P2Y1 receptors through apamin-sensitive K+ channels. EFS-induced on- and off-contractions are caused by stimulation of excitatory EMNs coreleasing ACh and tachykinins acting on muscular muscarinic and NK2 receptors. Prejunctional P2Y1 receptors might modulate the activity of excitatory EMNs. P2Y1 and NK2 receptors might be therapeutic targets for colonic motor disorders.British Journal of Pharmacology (2008) 155, 1043–1055; doi:10.1038/bjp.2008.332; published online 1 September 2008
Neurogastroenterology and Motility, 2010
Background Mechanoreceptors to the internal anal sphincter (IAS) contribute to continence and normal defecation, yet relatively little is known about their function or morphology. We investigated the function and structure of mechanoreceptors to the guinea pig IAS.Methods Extracellular recordings from rectal nerve branches to the IAS in vitro, combined with anterograde labeling of recorded nerve trunks, were used to characterize extrinsic afferent nerve endings activated by circumferential distension.Key Results Slowly adapting, stretch-sensitive afferents were recorded in rectal nerves to the IAS. Ten of 11 were silent under basal conditions and responded to circumferential stretch in a saturating linear manner. Rectal nerve afferents responded to compression with von Frey hairs with low thresholds (0.3–0.5 mN) and 3.4 ± 0.5 discrete, elongated mechanosensitive fields of innervation aligned parallel to circular muscle bundles (length = 62 ± 16 mm, n = 10). Anterogradely labeled rectal nerve axons typically passed through sparse irregular myenteric ganglia adjacent to the IAS, before ending in extensive varicose arrays within the circular muscle and, to a lesser extent, the longitudinal muscle overlying the IAS. Few (8%) IAS myenteric ganglia contained intraganglionic laminar endings. In eight preparations, mechanotransduction sites were mapped in combination with successful anterograde fills. Mechanotransduction sites were strongly associated with extensive fine varicose arrays within the circular muscle (P < 0.05), and not with any other neural structures.Conclusions & Inferences Mechanotransduction sites for low-threshold, slowly adapting mechanoreceptors innervating the IAS are likely to correspond to extensive fine varicose arrays within the circular muscle.