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Received November 19, 2004
Revised December 14, 2004
Accepted after revision January 6, 2005
1 The Johns Hopkins University School of Medicine
* To whom correspondence should be addressed. E-mail: bundem{at}jhmi.edu.
Some vagal afferent nerves are thought to mediate autonomic responses evoked by noxious oesophageal stimuli and participate in the perception of pain originating in 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 distention with pressure up to 100 mmHg) and detect noxious chemical stimuli (the capsaicin receptor TRPV1 activators). Using immunohistochemical techniques with retrogradely labeled 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 fibers. Vagal nociceptive-like fibres in guinea pig oesophagus are derived from two embryonically distinct sources. One source are neurones situated in the nodose vagal ganglia, the other are neurones situated in the jugular vagal ganglia. Nodose (placode-derived) nociceptive-like fibers are exclusively C-fibres sensitive to the P2X receptors agonist and rarely express neuropeptide substance P. In contrast, jugular (neural crest-derived) nociceptive-like fibers include both A- and C-fibres, are insensitive to the P2X receptors agonist and mostly express substance P. The non-nociceptive vagal tension mechanoreceptors are distinguished from nociceptors by their saturable response to oesophageal distention and by the lack of TRPV1. These tension mechanoreceptors are exclusively A-fibres arising from the nodose ganglion. We conclude that vagus nerves supply the guinea pig oesophagus with nociceptors in addition to tension mechanoreceptors. The vagal nociceptive-like fibres in the oesophagus comprise of two distinct subtypes dictated by the ganglionic location of their cell bodies.
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