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J Physiol Volume 582, Number 1, 229-242, July 1, 2007 DOI: 10.1113/jphysiol.2007.130823
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NEUROSCIENCE

Electrophysiological characterization of vagal afferents relevant to mucosal nociception in the rat upper oesophagus

J. K. M. Lennerz1,2, C. Dentsch2, N. Bernardini1, T. Hummel3, W. L. Neuhuber2 and P. W. Reeh1

1 Department of Physiology and Pathophysiology, Friedrich-Alexander-University Erlangen-Nürnberg, Universitätsstrasse 17, D-91054 Erlangen, Germany
2 Department of Anatomy I, Friedrich-Alexander-University Erlangen-Nürnberg, Krankenhausstasse 9, 91054, Erlangen, Germany
3 Department of Otorhinolaryngology, University of Dresden Medical School, Fetscherstrasse 74, 01307, Dresden, Germany

Emerging evidence indicates a nociceptive role of vagal afferents. A distinct oesophageal innervation in the rat, with muscular and mucosal afferents travelling predominantly in the recurrent (RLN) and superior laryngeal nerve (SLN), respectively, enabled characterization of mucosal afferents with nociceptive properties, using novel isolated oesophagus–nerve preparations. SLN and RLN single-fibre recordings identified 55 and 14 units, respectively, with none conducting faster than 8.7 m s–1. Mucosal response characteristics in the SLN distinguished mechanosensors (n = 13), mechanosensors with heat sensitivity (18) from those with cold sensitivity (19) and a mechanoinsensitive group (5). The mechanosensitive fibres, all slowly adapting, showed a unimodal distribution of mechanical thresholds (1.4–128 mN, peak ~5.7 mN). No difference in response characteristics of C and A{delta} fibres was encountered. Mucosal proton stimulation (pH 5.4 for 3 min), mimicking gastro-oesophageal reflux disease (GORD), revealed in 31% of units a desensitizing response that peaked around 20 s and faded within 60 s. Cold stimulation (15°C) was proportionally encoded but the response showed slow adaptation. In contrast, the noxious heat (48°C) response showed no obvious adaptation with discharge rates reflecting the temperature's time course. Polymodal (69%) mucosal units, > 30% proton sensitive, were found in each fibre category and were considered nociceptors; they are tentatively attributed to vagal nerve endings type I, IV and V, previously morphologically described. All receptive fields were mapped and the distribution indicates that the posterior upper oesophagus may serve as a ‘cutbank’, detecting noxious matters, ingested or regurgitated, and triggering nocifensive reflexes such as bronchoconstriction in GORD.

(Received 3 March 2007; accepted after revision 26 April 2007; first published online 3 May 2007)
Corresponding author P. W. Reeh: Department of Physiology and Pathophysiology, Friedrich-Alexander-University Erlangen-Nürnberg, Universitätsstrasse 17, 91054 Erlangen, Germany. Email: reeh{at}physiologie1.uni-erlangen.de


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