New insights into the organization of a gastroduodenal inhibitory reflex by the coeliac plexus

doi:10.1016/0165-1838(94)90150-3

Journal of the Autonomic Nervous System

Volume 46, Issues 1–2, January–February 1994, Pages 135-146

Journal of the Auton...

https://doi.org/10.1016/0165-1838(94)90150-3 Get rights and content

Abstract

The mechanisms involved at the prevertebral ganglionic level in a gastroduodenal inhibitory reflex were investigated in the rabbit on an in vitro preparation of the coeliac plexus connected to the stomach and duodenum. Intraluminal gastric and duodenal pressures were measured using water-filled balloons. Gastric distension inhibited duodenal motility via a nerve reflex which was abolished by section of the nerves connecting the coeliac plexus to the viscera. Superfusion of the coeliac plexus with a low Ca²⁺-high Mg²⁺ solution abolished the gastroduodenal inhibitory reflex, indicating a synaptic link at the ganglion level. The reflex was unaffected by superfusion of the coeliac plexus with hexamethonium and tubocurarine, ruling out a nicotinic mechanism. The reflex persisted when the coeliac plexus was superfused with tetrodotoxin or when the nerves connecting the coeliac plexus to the viscera were superfused with a Na⁺-free solution; these results indicate that the reflex does not involve sodium-dependent action potentials. Moreover, superfusion of the nerves connecting the coeliac plexus to the viscera with a calcium blocker or with a Ca²⁺-free solution also failed to abolish the reflex, suggesting that calcium-dependent action potentials are not involved. Our study demonstrates that a gastrointestinal inhibitory reflex via the coeliac ganglion is not based on fast synaptic inputs or action potentials. These results provide new insights concerning the physiology of the sympathetic prevertebral ganglia.

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Citation Excerpt :
Experiments of the last twenty years disclosed new complex function of these ganglia and nowadays prevertebral ganglia are considered to be an independent, autonomic nerve structures that are responsible for complex inter- and intra-organ regulations. Moreover, studies conducted in vivo have revealed that the celiac ganglion plays a crucial role in inhibitory reflex existing between the stomach and the duodenum (Mazet et al., 1994) as well as constitutes a connection between the central and peripheral nervous system (Simmons, 1985). Extrinsic sympathetic perikarya innervating the pylorus of the pig were found exclusively within the CSMG complex, and all of other prevertebral as well as paravertebral sympathetic ganglia were devoid of any FB-positive cells.
The pylorus, an important part of the digestive tract controlling the flow of chyme between the stomach and the duodenum, is widely innervated by intrinsic and extrinsic nerves. To determine the locations of postganglionic sympathetic perikarya that innervate the pylorus of the domestic pig, a retrograde tracing method with application of Fast Blue tracer was used. All positive neuronal cell bodies (ca. 1750) were found in the celiac-cranial mesenteric ganglion complex (CSMG), however, the coeliac poles of this complex provided the major input to the pylorus. Afterwards, the immunohistochemical staining procedure was applied to determine biologically active substances expressed in the FB-labeled perikarya. Approximately 77% of the FB-positive cell bodies contained tyrosine hydroxylase (TH), 87% dopamine β-hydroxylase (DβH), 40% neuropeptide Y (NPY), 12% somatostatin (SOM) and 7% galanin (GAL). The presence of all these substances in the ganglion tissue was confirmed by RT-PCR technique. Double immunocytochemistry revealed that all of the TH-positive perikarya contained DβH, about 40% NPY, 12% SOM and 8% GAL. Additionally, all above-cited immunohistochemical markers as well as VIP, PACAP, ChAT, LEU, MET, SP and nNOS were observed within nerve fibers associated with the FB-positive perikarya. Immunocytochemical labeling of the pyloric wall tissue disclosed that TH+, DβH+ and NPY+ nerve fibers innervated ganglia of the myenteric and submucosal plexuses, blood vessels, both muscular layers and the muscularis mucosae; nerve fibers immunoreactive to GAL mostly innervated both muscular layers, while SOM+ nerve fibers were observed within the myenteric plexus.
Presented study revealed sources of origin and immunohistochemical characteristics of the sympathetic postganglionic perikarya innervating the porcine pylorus.
From biological gastroenterology to fundamental neurosciences: How studies in gastric emptying have led to the discovery of a new mechanism of neuronal functioning
2010, Gastroenterologie Clinique et Biologique
Gastric emptying undergoes complex regulation by the nervous system, which organizes in particular the inhibition of duodenum motility after a rise in intra-gastric pressure: the gastro-duodenal inhibitory reflex. It was first shown in mammals that this reflex could be organized by a sympathetic ganglion, the coeliac plexus. The excitation of gastric mechanosensitive fibres leads in this ganglion to the release of a neurotransmitter, which in turn activates ganglionic neurones leading to inhibition of the duodenum contractions. It rapidly became apparent that this reflex presented striking properties since it was organized in the absence of action potentials along the nerve fibres. Then it was shown that the neurotransmitter released in the coeliac plexus was gaseous: nitric oxide (NO). The nature of the mechanism conducting, without action potentials, the excitation along the nerve fibres was recently determined. This mechanism necessitates the integrity of particular areas of the neuronal membrane (the lipid rafts) and the activation in cascade of the following second messenger sequence: ceramide, calcium, NO and guanosine cyclic monophosphate (c-GMP). These results show how studies in biological gastroenterology have led to the rethinking of one of the central dogmas in neuroscience according to which excitation is only conducted along the nerves by the action potential.
La vidange gastrique est régulée de manière complexe par le système nerveux. Celui-ci organise en particulier l’inhibition de la motricité duodénale après une augmentation de pression intragastrique : le réflexe gastro-duodénal inhibiteur. Il a initialement été montré chez le mammifère que ce réflexe peut être organisé par un ganglion sympathique, le plexus cœliaque. L’excitation des fibres gastriques mécanosensibles provoque la libération dans ce ganglion d’un neuromédiateur qui va activer des neurones ganglionnaires provoquant ainsi une inhibition du duodénum. Il est rapidement apparu que ce réflexe possède des propriétés atypiques puisqu’il est organisé en l’absence de potentiel d’action le long des fibres nerveuses. Puis il a été démontré que le neuromédiateur libéré dans le plexus cœliaque est gazeux : le monoxyde d’azote. La nature du mécanisme conduisant, sans potentiel d’action, l’excitation le long des fibres nerveuses a été déterminée récemment. Ce mécanisme nécessite l’intégrité de zones particulières de la membrane (les rafts lipidiques) et l’activation en cascade de la séquence de seconds messagers suivants : céramide, calcium, monoxyde d’azote et guanosine monophosphate cyclique. Ces résultats montrent comment des études en gastroentérologie biologique ont débouché sur la remise en cause d’un des dogmes majeurs des neurosciences qui stipule que l’excitation est uniquement transmise le long des nerfs par le potentiel d’action.
The mammalian sympathetic prevertebral ganglia: Models for the study of neuronal networks and basic neuronal properties
2009, Autonomic Neuroscience: Basic and Clinical
The mammalian sympathetic prevertebral ganglia regulate various visceral functions and in particular the digestive tract motility. Several integrative properties of these ganglia have been described: convergence of central inputs, projection of visceral inputs at the pre- and post synaptic level and pacemaker activity of the neurones. This review presents the results obtained on another integrative property which has been widely studied over the last 10 years: the modulation of the fast central inputs by neuromodulators such as nitric oxide, ceramide and GABA. These substances facilitate or inhibit the fast central inputs through complex interrelated actions. We also present striking results recently obtained during the study of a regulatory reflex of the digestive tract motility organized by the prevertebral ganglia: the gastro-duodenal inhibitory reflex. During this reflex, the neurotransmitter released by the visceral afferent fibres to activate the ganglionic neurones is gaseous: nitric oxide. Moreover, the mechanism conducting the excitation along the afferent and efferent fibres is independent of action potentials. This mechanism requires the integrity of the membrane lipid rafts and the activation in cascade of the following second messenger sequence: ceramide, calcium, nitric oxide and guanosine 3′, 5′-cyclic monophosphate. The existence of this mechanism gives grounds for rethinking one of the central dogmas in neuroscience according to which excitation is only conducted along nerves by an electrical phenomenon, the action potential. All these results strengthen the role of the prevertebral ganglia as a model for the study of neuronal networks and basic neuronal properties.
Small Intestinal Motility
2006, Physiology of the Gastrointestinal Tract

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Research paperNew insights into the organization of a gastroduodenal inhibitory reflex by the coeliac plexus

Abstract

Neuroscience

Brain Res.

Neuroscience

Brain Res.

Neuroscience

J. Auton. Nerv. Syst.

Neuroscience

Gastroenterology

Volume-sensitive synaptic input to neurons in guinea pig inferior mesenteric ganglion

Am. J. Physiol.

Local interneurones in insects

Excitatory input from the distal colon to the inferior mesenteric ganglion of the guinea-pig

J. Physiol.

A study of the inferior mesenteric and pelvic ganglia of guinea-pigs with intracellular electrodes

J. Physiol.

An intracellular characterization of neurones and neural connexions within the left coeliac ganglion of cats

J. Physiol.

Slow non-cholinergic excitatory potentials in neurones of the guinea-pig coeliac ganglia

J. Physiol.

Integration by spikeless neurones in the retina

Experimental investigation of visceral afferent synapses in coeliac ganglia

J. Neurophysiol.

Synaptic transmission without action potentials: input-output properties of a nonspiking presynaptic neuron

J. Neurophysiol.

An experimental analysis of the inferior mesenteric plexus

J. Comp. Neurol.

Electrophysiology of neurones of the inferior mesenteric ganglion of the cat

J. Physiol.

Venous mechanoreceptor input to neurones in the inferior mesenteric ganglion of the guinea-pig

J. Physiol.

Peripheral sympathetic pathways to gastroduodenal region of the guinea-pig

Am. J. Physiol.

Research paper
New insights into the organization of a gastroduodenal inhibitory reflex by the coeliac plexus