Characterization of excitatory and inhibitory motor neurons to the guinea pig lower esophageal sphincter

Brookes, Simon J.; Chen, B. N.; Hodgson, W. M.; Costa, Marcello

doi:10.1053/gast.1996.v111.pm8698189

Cited by 66 publications

(51 citation statements)

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“…In addition, all of these functional studies and our present results on humans agree with morphological studies mapping the regional distribution of EMNs in guinea pig LES that found that, in the clasp region, 33% of the neurons stain positively for cholineacetyl-transferase, whereas 70% stain positively for NO synthase (2). In contrast, sling fibers are mainly innervated (Ͼ80%) by cholinergic neurons, with only 15% staining positively for NO synthase (40,2). Taken together with our previous functional studies, all of these findings strongly suggest that, in the human LES, the inhibitory neurons predominate in the clasp, whereas the excitatory ones predominate in the sling fibers.…”

Section: Discussionsupporting

confidence: 91%

“…Supporting our results on both humans and pigs, studies on the guinea pig LES also show a marked functional neural asymmetry, as vagal stimulation causes activation of excitatory and inhibitory EMNs on the sling LES side (40) and only inhibitory responses in the clasp (39). In addition, all of these functional studies and our present results on humans agree with morphological studies mapping the regional distribution of EMNs in guinea pig LES that found that, in the clasp region, 33% of the neurons stain positively for cholineacetyl-transferase, whereas 70% stain positively for NO synthase (2). In contrast, sling fibers are mainly innervated (Ͼ80%) by cholinergic neurons, with only 15% staining positively for NO synthase (40,2).…”

Section: Discussionsupporting

confidence: 89%

“…Animal studies described that NO released from inhibitory myenteric neurons controlled both the amplitude and the latency timing of the off-response in the distal smooth muscle esophagus (5) and mediated nerve-induced hyperpolarization of circular esophageal and LES smooth muscle (4, 6). These in vitro animal studies also found that inhibition of NOS with L-NNA or by blocking the NO-intracellular pathway with the guanylate cyclase inhibitor 1H- [1,2,4]oxadiazolo- [4,3-a]quinoxalin-1-one attenuated or even abolished the off-response and shortened the latency period, inducing the appearance of a cholinergic on-contraction of greater amplitude than the previous on-and off-contractions (5,20). In our human study, in vitro on and off EB contractions are similar to these previous in vitro animal studies and to the two types of esophageal peristaltic contractions found during in vivo vagal stimulation in the opossum esophagus (20).…”

Section: Discussionmentioning

confidence: 82%

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Regional functional specialization and inhibitory nitrergic and nonnitrergic coneurotransmission in the human esophagus

Lecea

Gallego

Farré

et al. 2011

American Journal of Physiology-Gastrointestinal and Liver Physi

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Lecea B, Gallego D, Farré R, Opazo A, Aulí M, Jiménez M, Clavé P. Regional functional specialization and inhibitory nitrergic and nonnitrergic coneurotransmission in the human esophagus. Am J Physiol Gastrointest Liver Physiol 300: G782-G794, 2011. First published February 17, 2011 doi:10.1152/ajpgi.00514.2009.-The aim of this study was to explore the myenteric mechanisms of control of human esophageal motility and the effect of nitrergic and nonnitrergic neurotransmitters. Human circular esophageal strips were studied in organ baths and with microelectrodes. Responses following electrical field stimulation (EFS) of enteric motoneurons (EMNs) or through nicotinic acetylcholine receptors were compared in the esophageal body (EB) and in clasp and sling regions in the lower esophageal sphincter (LES). In clasp LES strips: 1) sodium nitroprusside (1 nM to 100 M), adenosine-5=-[␤-thio]diphosphate trilithium salt (1-100 M), and vasoactive intestinal peptide (1 nM to 1 M) caused a relaxation; 2) 1 mM N -nitro-L-arginine (L-NNA) shifted the EFS "on"-relaxation to an "off"-relaxation, partly antagonized by 10 M 2=-deoxy-N 6 -methyladenosine 3=,5=-bisphosphate tetrasodium salt (MRS2179) or 10 U/ml ␣-chymotrypsin; and 3) nicotine-relaxation (100 M) was mainly antagonized by L-NNA, and only partly by MRS2179 or ␣-chymotrypsin. In sling LES fibers, EFS and nicotine relaxation was abolished by L-NNA. In the EB, L-NNA blocked the latency period, and MRS2179 reduced "off"-contraction. The amplitude of cholinergic contraction decreased from the EB to both LES sides. EFS induced a monophasic inhibitory junction potential in clasp, sling, and EB fibers abolished by L-NNA. Our study shows a regional specialization to stimulation of EMNs in the human esophagus, with stronger inhibitory responses in clasp LES fibers and stronger cholinergic excitatory responses in the EB. Inhibitory responses are mainly triggered by nitrergic EMNs mediating the inhibitory junction potentials in the LES and EB, EFS on-relaxation in clasp and sling LES sides, and latency in the EB. We also found a minor role for purines (through P2Y1 receptors) and vasoactive intestinal peptide-mediating part of nonnitrergic clasp LES relaxation. lower esophageal sphincter; esophageal body; inhibitory motoneurons; inhibitory coneurotransmission THE MAIN PHYSIOLOGICAL FUNCTION of the lower esophageal sphincter (LES) is to generate a zone of high pressure that prevents the reflux of acid gastric content into the esophagus. LES relaxations occur briefly after swallowing, and transient LES relaxations cause physiological gastroesophageal reflux and allow belching. Enteric motoneurons (EMNs) are the final step in the inhibitory vagal pathway to the LES, mediating swallow-induced and transient LES relaxation (3). Nitric oxide (NO) released from these inhibitory EMNs is the major contributor to LES relaxation in humans (12) and opossums (20, 33). However, vasoactive intestinal peptide (VIP) and ATP are putative inhibitory neurotransmitters in animal studies (14, 21-24, 34, ...

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 89%

Section: Discussionmentioning

confidence: 82%

See 1 more Smart Citation

Regional functional specialization and inhibitory nitrergic and nonnitrergic coneurotransmission in the human esophagus

Lecea

Gallego

Farré

et al. 2011

American Journal of Physiology-Gastrointestinal and Liver Physi

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“…All of these functional data, including the present results, agree with morphological studies in guinea-pig LOS where the density of EMNs was low in the clasp region and the majority were inhibitory 9 , compared with the sling region where the density of EMNs was four times greater and the majority (79 per cent) were cholinergic 8,10 .…”

Section: Discussionsupporting

confidence: 91%

Mechanisms controlling function in the clasp and sling regions of porcine lower oesophageal sphincter

Farré

Aulí

Lecea

et al. 2007

British Journal of Surgery

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“…The ChAT antiserum (P03 Yeboah, Schemann, Munich, Germany) was reported to label authentic ChAT in guinea pig gastrointestinal tract (Schemann et al, 1993;Schemann and Schaaf, 1995) and has been used to label cholinergic excitatory motor neurons in the gut wall (Brookes et al, 1996(Brookes et al, , 1998. The ChAT antiserum (No.…”

Section: Antibody Characterizationmentioning

confidence: 99%

Comparison of extrinsic efferent innervation of guinea pig distal colon and rectum

et al. 2006

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The extrinsic efferent innervation of the distal colon and rectum of the guinea pig was compared, by using retrograde tracing combined with immunohistochemistry. Application of the carbocyanine tracer DiI to the rectum filled significantly greater numbers of extrinsic neurons than similar injections into the distal colon. Approximately three-fourths of all filled neurons from either location were either sympathetic or parasympathetic; the rest were spinal sensory neurons. Nerve cell bodies in sympathetic prevertebral ganglia labelled from the two regions were similar in number. Both regions were innervated by sympathetic neurons in paravertebral ganglia; however, the rectum received much more input from this source than the colon. The rectum received significantly more input from pelvic ganglia than the colon. The rectum also received direct innervation from two groups of neurons in the spinal cord. Neurons located in the spinal parasympathetic nucleus in segment S2 and S3 were labelled by DiI injected into the rectal wall. Similar numbers of neurons, located in intermediolateral cell column and dorsal commissural nucleus of lumbar segments, also projected directly to rectum, but not colon. The great majority (>80%) of retrogradely labelled nerve cell bodies in sympathetic ganglia were immunoreactive for tyrosine hydroxylase. In pelvic ganglia, retrogradely labelled neurons contained choline acetyltransferase and/or nitric oxide synthase or tyrosine hydroxylase. Although the rectum and colon in this species are continuous and macroscopically indistinguishable, they have significantly different patterns of extrinsic efferent innervation, presumably reflecting their different functions.

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Characterization of excitatory and inhibitory motor neurons to the guinea pig lower esophageal sphincter

Cited by 66 publications

References 1 publication

Regional functional specialization and inhibitory nitrergic and nonnitrergic coneurotransmission in the human esophagus

Regional functional specialization and inhibitory nitrergic and nonnitrergic coneurotransmission in the human esophagus

Mechanisms controlling function in the clasp and sling regions of porcine lower oesophageal sphincter

Comparison of extrinsic efferent innervation of guinea pig distal colon and rectum

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