Vagal afferent nerves with nociceptive properties in guinea-pig oesophagus

Shaoyong Yu, Bradley J Undem, Marian Kollarik

Research output: Contribution to journalArticle

Abstract

Some vagal afferent nerves are thought to mediate autonomic responses evoked by noxious oesophageal stimuli and participate in the perception of pain originating in the oesophagus. However, the vagal nociceptive nerve phenotypes implicated in this function have yet to be identified. In this study, nociceptive fibres were defined by the capacity to discriminate noxious mechanical stimuli (wide range of oesophageal distension with pressure up to 100 mmHg) and detect noxious chemical stimuli (the activators of capsaicin receptor TRPV1). Using immunohistochemical techniques with retrogradely labelled oesophagus-specific neurones and performing extracellular recordings from the isolated vagally innervated oesophagus, we show that in the guinea-pig, the vagus nerves supply the oesophagus with a large population of nociceptive-like afferent nerve fibres. Vagal nociceptive-like fibres in the guinea-pig oesophagus are derived from two embryonically distinct sources: neurones situated in the nodose vagal ganglia and neurones situated in the jugular vagal ganglia. Nodose (placode-derived) nociceptive-like fibres are exclusively C-fibres sensitive to a P2X receptors agonist and rarely express the neuropeptide substance P. In contrast, jugular (neural crest-derived) nociceptive-like fibres include both A-fibres and C-fibres, are insensitive to P2X receptors agonist and mostly express substance P. The non-nociceptive vagal tension mechanoreceptors are distinguished from nociceptors by their saturable response to oesophageal distension and by the lack of TRPV1. These tension mechanoreceptors are exclusively A-fibres arising from the nodose ganglion. We conclude that the vagus nerves supply the guinea-pig oesophagus with nociceptors in addition to tension mechanoreceptors. The vagal nociceptive-like fibres in the oesophagus comprise two distinct subtypes dictated by the ganglionic location of their cell bodies.

Original languageEnglish (US)
Pages (from-to)831-842
Number of pages12
JournalJournal of Physiology
Volume563
Issue number3
DOIs
StatePublished - Mar 15 2005

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Esophagus
Guinea Pigs
Mechanoreceptors
Nodose Ganglion
Myelinated Nerve Fibers
Unmyelinated Nerve Fibers
Nociceptors
Vagus Nerve
Substance P
Neurons
Neck
TRPV Cation Channels
Pain Perception
Neural Crest
Neuropeptides
Nerve Fibers
Ganglia
Phenotype
Pressure
Population

ASJC Scopus subject areas

  • Physiology

Cite this

Vagal afferent nerves with nociceptive properties in guinea-pig oesophagus. / Yu, Shaoyong; Undem, Bradley J; Kollarik, Marian.

In: Journal of Physiology, Vol. 563, No. 3, 15.03.2005, p. 831-842.

Research output: Contribution to journalArticle

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