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

• Published in: The Journal of physiology Vol. 582; no. 1; pp. 229 - 242
• Main Authors: Lennerz, J. K. M., Dentsch, C., Bernardini, N., Hummel, T., Neuhuber, W. L., Reeh, P. W.
• Format: Journal Article
• Language: English
• Published: Oxford, UK The Physiological Society 01-07-2007; Blackwell Publishing Ltd; Blackwell Science Inc
• Subjects: Action Potentials; Animals; Cold Temperature; Electrophysiology - methods; Esophagus - innervation; Esophagus - metabolism; Gastroesophageal Reflux - complications; Gastroesophageal Reflux - metabolism; Gastroesophageal Reflux - physiopathology; Hot Temperature; Hydrogen-Ion Concentration; In Vitro Techniques; Kinetics; Laryngeal Nerves - metabolism; Male; Mechanotransduction, Cellular; Mucous Membrane - innervation; Mucous Membrane - metabolism; Muscle, Smooth - innervation; Muscle, Smooth - metabolism; Neural Conduction; Neurons, Afferent - metabolism; Neuroscience; Nociceptors - metabolism; Pain - etiology; Pain - metabolism; Pain - physiopathology; Rats; Rats, Wistar; Reaction Time; Recurrent Laryngeal Nerve - metabolism; Sensory Thresholds; Skin - innervation; Vagus Nerve - cytology; Vagus Nerve - metabolism
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.2007.130823

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 Aδ 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.