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. 1996 Oct 15;496(Pt 2):521–530. doi: 10.1113/jphysiol.1996.sp021703

Interganglionic segregation of distinct vagal afferent fibre phenotypes in guinea-pig airways.

M M Ricco 1, W Kummer 1, B Biglari 1, A C Myers 1, B J Undem 1
PMCID: PMC1160895  PMID: 8910234

Abstract

1. The present study addressed the hypothesis that jugular and nodose vagal ganglia contain the somata of functionally and anatomically distinct airway afferent fibres. 2. Anatomical investigations were performed by injecting guinea-pig airways with the neuronal tracer Fast Blue. The animals were killed 7 days later, and the ganglia were removed and immunostained with antisera against substance P (SP) and neurofilament protein (NF). In the nodose ganglion, NF-immunoreactive neurones accounted for about 98% of the Fast Blue-labelled cells while in the jugular ganglion they accounted for approximately 48%. SP and NF immunoreactivity was never (n = 100) observed in the same cell suggesting that the antisera labelled distinct populations. 3. Electrophysiological investigations were performed using an in vitro guinea-pig tracheal and bronchial preparation with intact afferent vagal pathways, including nodose and jugular ganglia. Action potentials arriving from single airway afferent nerve endings were monitored extracellularly using a glass microelectrode positioned near neuronal cell bodies in either ganglion. 4. The nodose ganglion contained the somata of mainly fast-conducting tracheal A delta fibres whereas the jugular ganglion contained equal numbers of C fibre and A delta fibre tracheal afferent somata. The nodose A delta neurones adapted rapidly to mechanical stimulation, had relatively low mechanical thresholds, were not activated by capsaicin and adapted rapidly to a hyperosmotic stimulus. By contrast, jugular A delta and C fibres adapted slowly to mechanical stimulation, were often activated by capsaicin, had higher mechanical thresholds and displayed a slow adaptation to a hyperosmotic stimulus. 5. The anatomical, physiological and pharmacological data provide evidence to support the contention that the vagal ganglionic source of the fibre supplying the airways ultimately dictates its neurochemical and physiological phenotype.

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Selected References

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  1. AGOSTONI E., CHINNOCK J. E., DE DALY M. B., MURRAY J. G. Functional and histological studies of the vagus nerve and its branches to the heart, lungs and abdominal viscera in the cat. J Physiol. 1957 Jan 23;135(1):182–205. doi: 10.1113/jphysiol.1957.sp005703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armstrong D. J., Luck J. C. A comparative study of irritant and type J receptors in the cat. Respir Physiol. 1974 Jul;21(1):47–60. doi: 10.1016/0034-5687(74)90006-1. [DOI] [PubMed] [Google Scholar]
  3. Bałuk P., Gabella G. Innervation of the guinea pig trachea: a quantitative morphological study of intrinsic neurons and extrinsic nerves. J Comp Neurol. 1989 Jul 1;285(1):117–132. doi: 10.1002/cne.902850110. [DOI] [PubMed] [Google Scholar]
  4. Canning B. J., Undem B. J. Evidence that distinct neural pathways mediate parasympathetic contractions and relaxations of guinea-pig trachealis. J Physiol. 1993 Nov;471:25–40. doi: 10.1113/jphysiol.1993.sp019889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Canning B. J., Undem B. J. Relaxant innervation of the guinea-pig trachealis: demonstration of capsaicin-sensitive and -insensitive vagal pathways. J Physiol. 1993 Jan;460:719–739. doi: 10.1113/jphysiol.1993.sp019496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coleridge H. M., Coleridge J. C. Pulmonary reflexes: neural mechanisms of pulmonary defense. Annu Rev Physiol. 1994;56:69–91. doi: 10.1146/annurev.ph.56.030194.000441. [DOI] [PubMed] [Google Scholar]
  7. Coleridge J. C., Coleridge H. M. Afferent vagal C fibre innervation of the lungs and airways and its functional significance. Rev Physiol Biochem Pharmacol. 1984;99:1–110. doi: 10.1007/BFb0027715. [DOI] [PubMed] [Google Scholar]
  8. Dalsgaard C. J., Lundberg J. M. Evidence for a spinal afferent innervation of the guinea pig lower respiratory tract as studied by the horseradish peroxidase technique. Neurosci Lett. 1984 Mar 23;45(2):117–122. doi: 10.1016/0304-3940(84)90085-5. [DOI] [PubMed] [Google Scholar]
  9. Davies R. O., Kubin L. Projection of pulmonary rapidly adapting receptors to the medulla of the cat: an antidromic mapping study. J Physiol. 1986 Apr;373:63–86. doi: 10.1113/jphysiol.1986.sp016035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dey R. D., Altemus J. B., Zervos I., Hoffpauir J. Origin and colocalization of CGRP- and SP-reactive nerves in cat airway epithelium. J Appl Physiol (1985) 1990 Feb;68(2):770–778. doi: 10.1152/jappl.1990.68.2.770. [DOI] [PubMed] [Google Scholar]
  11. Donoghue S., Garcia M., Jordan D., Spyer K. M. The brain-stem projections of pulmonary stretch afferent neurones in cats and rabbits. J Physiol. 1982 Jan;322:353–363. doi: 10.1113/jphysiol.1982.sp014041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. EVANS D. H., MURRAY J. G. Histological and functional studies on the fibre composition of the vagus nerve of the rabbit. J Anat. 1954 Jul;88(3):320–337. [PMC free article] [PubMed] [Google Scholar]
  13. Forssmann W. G., Ito S., Weihe E., Aoki A., Dym M., Fawcett D. W. An improved perfusion fixation method for the testis. Anat Rec. 1977 Jul;188(3):307–314. doi: 10.1002/ar.1091880304. [DOI] [PubMed] [Google Scholar]
  14. Fox A. J., Barnes P. J., Dray A. Stimulation of guinea-pig tracheal afferent fibres by non-isosmotic and low-chloride stimuli and the effect of frusemide. J Physiol. 1995 Jan 1;482(Pt 1):179–187. doi: 10.1113/jphysiol.1995.sp020508. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fox A. J., Barnes P. J., Urban L., Dray A. An in vitro study of the properties of single vagal afferents innervating guinea-pig airways. J Physiol. 1993 Sep;469:21–35. doi: 10.1113/jphysiol.1993.sp019802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. HOLMES R., TORRANCE R. W. Afferent fibres of the stellate ganglion. Q J Exp Physiol Cogn Med Sci. 1959 Jul;44:271–281. doi: 10.1113/expphysiol.1959.sp001400. [DOI] [PubMed] [Google Scholar]
  17. Holzer P. Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol Rev. 1991 Jun;43(2):143–201. [PubMed] [Google Scholar]
  18. Kummer W., Fischer A., Kurkowski R., Heym C. The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry. Neuroscience. 1992 Aug;49(3):715–737. doi: 10.1016/0306-4522(92)90239-x. [DOI] [PubMed] [Google Scholar]
  19. Lawson S. N., Waddell P. J. Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons. J Physiol. 1991 Apr;435:41–63. doi: 10.1113/jphysiol.1991.sp018497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maggi C. A. The pharmacology of the efferent function of sensory nerves. J Auton Pharmacol. 1991 Jun;11(3):173–208. doi: 10.1111/j.1474-8673.1991.tb00317.x. [DOI] [PubMed] [Google Scholar]
  21. McCarthy P. W., Lawson S. N. Cell type and conduction velocity of rat primary sensory neurons with substance P-like immunoreactivity. Neuroscience. 1989;28(3):745–753. doi: 10.1016/0306-4522(89)90019-5. [DOI] [PubMed] [Google Scholar]
  22. McDonald D. M., Mitchell R. A., Gabella G., Haskell A. Neurogenic inflammation in the rat trachea. II. Identity and distribution of nerves mediating the increase in vascular permeability. J Neurocytol. 1988 Oct;17(5):605–628. doi: 10.1007/BF01260989. [DOI] [PubMed] [Google Scholar]
  23. Mohammed S. P., Higenbottam T. W., Adcock J. J. Effects of aerosol-applied capsaicin, histamine and prostaglandin E2 on airway sensory receptors of anaesthetized cats. J Physiol. 1993 Sep;469:51–66. doi: 10.1113/jphysiol.1993.sp019804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Riccio M. M., Myers A. C., Undem B. J. Immunomodulation of afferent neurons in guinea-pig isolated airway. J Physiol. 1996 Mar 1;491(Pt 2):499–509. doi: 10.1113/jphysiol.1996.sp021234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sant'Ambrogio G. Nervous receptors of the tracheobronchial tree. Annu Rev Physiol. 1987;49:611–627. doi: 10.1146/annurev.ph.49.030187.003143. [DOI] [PubMed] [Google Scholar]
  26. Springall D. R., Cadieux A., Oliveira H., Su H., Royston D., Polak J. M. Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J Auton Nerv Syst. 1987 Aug;20(2):155–166. doi: 10.1016/0165-1838(87)90113-5. [DOI] [PubMed] [Google Scholar]
  27. Undem B. J., Weinreich D. Electrophysiological properties and chemosensitivity of guinea pig nodose ganglion neurons in vitro. J Auton Nerv Syst. 1993 Jul;44(1):17–33. doi: 10.1016/0165-1838(93)90375-5. [DOI] [PubMed] [Google Scholar]
  28. WIDDICOMBE J. G. Receptors in the trachea and bronchi of the cat. J Physiol. 1954 Jan;123(1):71–104. doi: 10.1113/jphysiol.1954.sp005034. [DOI] [PMC free article] [PubMed] [Google Scholar]

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