Release of nitric oxide within the coeliac plexus is involved in the organization of a gastroduodenal inhibitory reflex in the rabbit

Abstract

The autonomic nervous system is involved in the regulation of visceral function, including the regulation of digestive tract motility. One characteristic of this system is that the nervous regulatory structures are not localized exclusively in the cerebrospinal axis. From a classic point of view, it could be described as having an intrinsic level of regulation located in the viscera and an extrinsic level of regulation in the prevertebral ganglia and central nervous structures, with each level of regulation having its own integrative properties. The prevertebral ganglia, which are part of the sympathetic system, have long been considered as a simple relay on the efferent central pathway. During the last 20 years, numerous studies devoted to the prevertebral ganglia have shown that they behave as true integrative nervous structures able to organize intra-and interorgan regulation.Experiments performed on in vitro preparations consisting of prevertebral ganglia connected to part of the digestive tract have revealed the involvement of these ganglia in the organization of gastrointestinal reflexes. Kreulen & Szurszewski (1979) showed that an inhibitory reflex occurred between two segments of the colon connected only via the coeliac ganglion and the inferior mesenteric ganglion by the mesenteric nerves. This reflex disappeared after sectioning of the intermesenteric nerves. Inhibitory gastrointestinal reflexes organized by the coeliac plexus have also been demonstrated in in vitro models consisting of isolated stomach and duodenum connected only to the coeliac plexus by nervous rami (Kreulen et al. 1983;Mazet et al. 1993b). In a previous study (Mazet et al. 1993b), we demonstrated that a delayed and long-lasting gastrointestinal inhibitory reflex was organized by the coeliac plexus. This nervous Journal of Physiology (1999) 1. The coeliac plexus can organize a gastroduodenal inhibitory reflex without action potentials. The involvement of the nitric oxide-cGMP pathway in this reflex was investigated in the rabbit on an in vitro preparation of the coeliac plexus connected to the stomach and duodenum. Intraluminal duodenal pressures were measured with water-filled balloons. Gastric distension inhibited duodenal motility, thus characterizing a gastroduodenal inhibitory reflex organized by the coeliac plexus. 2. ¬_Arginine, superfused at the coeliac plexus level, enhanced this reflex, whereas N ù -nitro¬_arginine (¬-NOARG) or 2-(4-carboxyphenyl)-4,4,5,5tetramethylimidazoline-1-oxyl-3-oxide (carboxyPTIO) reduced or abolished it. Moreover, diethylamineÏnitric oxide complex superfused at the coeliac plexus level inhibited duodenal motility in the absence of gastric distension. 3. The effects of nitric oxide were mediated through the activation of guanylyl cyclase, as 1H_[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ) reduced or abolished the gastroduodenal inhibitory reflex, whereas zaprinast enhanced it. Moreover, 8-bromo-cGMP and cGMP, superfused at the coeliac plexus level, inhibited duodenal motility in the absence of gas...

Neuronal Conduction of Excitation without Action Potentials Based on Ceramide Production

“…This explains why the conduction of excitation remains limited to the specific network activated by gastric distension. In a previous work we have shown that superfusion of the coeliac plexus with carboxyPTIO inhibited the GIR [2]. This indicated that NO is the neurotransmitter released in the extracellular space by the gastric afferent fibres to activate the ganglionic neurons.…”

“…When the nerve trunks were selectively superfused with 2 µM 1H-[1], [2], [4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ, a selective inhibitor of the NO-activated soluble guanylate cyclase) for at least 30 min, the gastric distension failed to affect the duodenal contractions significantly (paired t test, non significant, df = 3, Fig. 4f).…”

“…We first provided pharmacological and electrophysiological evidence that this reflex is organized without action potentials along the autonomic nerve fibres by an unconventional mechanism of excitation which remains unexplained [1]. We then provided pharmacological evidence that during GIR, the neurotransmitter released by the afferent fibres to activate the ganglion neurons is nitric oxide (NO) [2].…”

Localization and neurochemical characteristics of the extrinsic sympathetic neurons projecting to the pylorus in the domestic pig

“…More precise data concern only fibers secreting nitric oxide (NO). Experiments in rabbits revealed a strong involvement of NO, released in the region of CSMG complex, in the gastro-duodenal inhibitory reflex (Quinson et al, 1999(Quinson et al, , 2000. It was also hypothesized that NO triggers activation of the cyclic guanosine monophosphate (cGMP) pathway in the target cells (Anderson et al, 1994;Quinson et al, 2000).…”

Conduction nerveuse d’excitation sans potentiel d’action

“…Notre étude a été effectuée sur une préparation in vitro composée d'un centre nerveux périphérique, le plexus coeliaque [2], connecté à l'estomac et au duodénum (Figure 1). Nous avons ensuite établi que le neuromédiateur libéré dans le plexus coeliaque lors de ce fonctionnement neuronal non conventionnel est un gaz, le monoxyde d'azote (NO) [3]. À ce stade de nos recherches le mécanisme de Cependant ces radeaux n'avaient encore jamais été mis en évidence dans les élé-ments périphériques du système nerveux végétatif.…”