Brainstem pathways responsible for oesophageal control of gastric motility and tone in the rat

R. C. Rogers, G. E. Hermann, R. A. Travagli

Research output: Contribution to journalArticle

117 Citations (Scopus)

Abstract

1. Previous anatomical studies indicate that the nucleus of the solitary tract, pars centralis (NSTc) contains the neurones which receive vagal afferent input from the oesophagus. The purpose of the present study was to characterize the NSTc circuits in the medulla that may be responsible for oesophageal control of gastric motility. 2. Moderate balloon distension of the oesophagus of the rat (14-18 mmHg) provoked a significant reduction in gastric motility and tone recorded with strain gauges. This receptive relaxation effect was eliminated by bilateral lesions centred on the NSTc. NSTc cells activated by oesophageal distension were labelled extracellularly and juxtacellularly with neurobiotin. NSTc neurones send axonal projections throughout the entire rostral-caudal extent of the dorsal motor nucleus of the vagus (DMN). These NSTc-DMN connections were confirmed by retrograde transport of neurobiotin from DMN to NSTc. NSTc neurones were observed with dendrites arborizing within the ependymal lining of the fourth ventricles. Thus, NSTc neurones may be in position to monitor blood-borne or ventricular agents and to alter the function of gastric-vago-vagal reflexes in response to these stimuli. 4. Neurophysiological recordings identified two subpopulations of DMN neurones which may be either activated or inhibited by oesophageal distension. Neurones excited by oesophageal distension were located mainly lateral and caudal in the DMN; neurones inhibited by oesophageal stimulation were located in medial and rostral DMN. 5. Our neurobiotin tracing results verified earlier studies showing that the NSTc projects to the intermediate reticular nucleus and the compact division of the nucleus ambiguus. Additionally, we found that the NSTc may be involved in reciprocal connections with the anterior, rostrolateral NST. 6. These results suggest that the gastric relaxation evoked by oesophageal distension is critically dependent on intact brainstem vago-vagal circuits. The NSTc, the recipient of oesophageal afferent projections from the vagus nerve, sends axons to the entire DMN, the source of parasympathetic control of the stomach. DMN neurones respond differentially to oesophageal distension, reinforcing the view that oesophageal afferents may provoke gastric relaxation by activating a vagal inhibitory pathway while simultaneously inhibiting a vagal excitatory pathway.

Original languageEnglish (US)
Pages (from-to)369-383
Number of pages15
JournalJournal of Physiology
Volume514
Issue number2
DOIs
StatePublished - Jan 15 1999

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Solitary Nucleus
Brain Stem
Stomach
Neurons
Esophagus
Fourth Ventricle
Medulla Oblongata
Vagus Nerve
Dendrites
Axons
Reflex

All Science Journal Classification (ASJC) codes

  • Physiology

Cite this

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abstract = "1. Previous anatomical studies indicate that the nucleus of the solitary tract, pars centralis (NSTc) contains the neurones which receive vagal afferent input from the oesophagus. The purpose of the present study was to characterize the NSTc circuits in the medulla that may be responsible for oesophageal control of gastric motility. 2. Moderate balloon distension of the oesophagus of the rat (14-18 mmHg) provoked a significant reduction in gastric motility and tone recorded with strain gauges. This receptive relaxation effect was eliminated by bilateral lesions centred on the NSTc. NSTc cells activated by oesophageal distension were labelled extracellularly and juxtacellularly with neurobiotin. NSTc neurones send axonal projections throughout the entire rostral-caudal extent of the dorsal motor nucleus of the vagus (DMN). These NSTc-DMN connections were confirmed by retrograde transport of neurobiotin from DMN to NSTc. NSTc neurones were observed with dendrites arborizing within the ependymal lining of the fourth ventricles. Thus, NSTc neurones may be in position to monitor blood-borne or ventricular agents and to alter the function of gastric-vago-vagal reflexes in response to these stimuli. 4. Neurophysiological recordings identified two subpopulations of DMN neurones which may be either activated or inhibited by oesophageal distension. Neurones excited by oesophageal distension were located mainly lateral and caudal in the DMN; neurones inhibited by oesophageal stimulation were located in medial and rostral DMN. 5. Our neurobiotin tracing results verified earlier studies showing that the NSTc projects to the intermediate reticular nucleus and the compact division of the nucleus ambiguus. Additionally, we found that the NSTc may be involved in reciprocal connections with the anterior, rostrolateral NST. 6. These results suggest that the gastric relaxation evoked by oesophageal distension is critically dependent on intact brainstem vago-vagal circuits. The NSTc, the recipient of oesophageal afferent projections from the vagus nerve, sends axons to the entire DMN, the source of parasympathetic control of the stomach. DMN neurones respond differentially to oesophageal distension, reinforcing the view that oesophageal afferents may provoke gastric relaxation by activating a vagal inhibitory pathway while simultaneously inhibiting a vagal excitatory pathway.",
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Brainstem pathways responsible for oesophageal control of gastric motility and tone in the rat. / Rogers, R. C.; Hermann, G. E.; Travagli, R. A.

In: Journal of Physiology, Vol. 514, No. 2, 15.01.1999, p. 369-383.

Research output: Contribution to journalArticle

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N2 - 1. Previous anatomical studies indicate that the nucleus of the solitary tract, pars centralis (NSTc) contains the neurones which receive vagal afferent input from the oesophagus. The purpose of the present study was to characterize the NSTc circuits in the medulla that may be responsible for oesophageal control of gastric motility. 2. Moderate balloon distension of the oesophagus of the rat (14-18 mmHg) provoked a significant reduction in gastric motility and tone recorded with strain gauges. This receptive relaxation effect was eliminated by bilateral lesions centred on the NSTc. NSTc cells activated by oesophageal distension were labelled extracellularly and juxtacellularly with neurobiotin. NSTc neurones send axonal projections throughout the entire rostral-caudal extent of the dorsal motor nucleus of the vagus (DMN). These NSTc-DMN connections were confirmed by retrograde transport of neurobiotin from DMN to NSTc. NSTc neurones were observed with dendrites arborizing within the ependymal lining of the fourth ventricles. Thus, NSTc neurones may be in position to monitor blood-borne or ventricular agents and to alter the function of gastric-vago-vagal reflexes in response to these stimuli. 4. Neurophysiological recordings identified two subpopulations of DMN neurones which may be either activated or inhibited by oesophageal distension. Neurones excited by oesophageal distension were located mainly lateral and caudal in the DMN; neurones inhibited by oesophageal stimulation were located in medial and rostral DMN. 5. Our neurobiotin tracing results verified earlier studies showing that the NSTc projects to the intermediate reticular nucleus and the compact division of the nucleus ambiguus. Additionally, we found that the NSTc may be involved in reciprocal connections with the anterior, rostrolateral NST. 6. These results suggest that the gastric relaxation evoked by oesophageal distension is critically dependent on intact brainstem vago-vagal circuits. The NSTc, the recipient of oesophageal afferent projections from the vagus nerve, sends axons to the entire DMN, the source of parasympathetic control of the stomach. DMN neurones respond differentially to oesophageal distension, reinforcing the view that oesophageal afferents may provoke gastric relaxation by activating a vagal inhibitory pathway while simultaneously inhibiting a vagal excitatory pathway.

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