Skip to main content

Structure of Airway Smooth Muscle and Its Innervation

  • Chapter
Airway Smooth Muscle in Health and Disease

Abstract

The musculature of the trachea and bronchi is well supplied with nerves; its activity is under myogenic control as well as under nervous and hormonal control. The main source of afferent fibers to trachea and bronchi are nerve cells in the nodose ganglion whose axons reach the trachea through the recurrent laryngeal nerve; whether there are also some afferent fibers from dorsal root ganglia remains to be proved—a possibility suggested by Dalsgaard and Lundberg (1984). The vagal (afferent) fibers represent the largest nerve supply to the bronchial and tracheal muscles of the mouse, as judged by the extent of the loss of intramuscular nerve endings after vagotomy (Pack et al., 1984). The main source of efferent fibers are ganglion cells in the tracheal and bronchial ganglia (see Chapter this volume) and possibly in some other of the many ganglia associated with mediastinal organs. These neurons are driven (exclusively?) by vagal preganglionic nerve fibers and are part of the parasympathetic outflow; they include excitatory and inhibitory neurons. In the ferret, axons projecting from these neurons to the tracheal muscle have been traced after intracellular injection of horseradish peroxidase (HRP) (Kalia et al., 1983). Efferent vagal fibers are preganglionic and do not reach the musculature, but they all end within the ganglia. There are on average 235 neurons in the ganglionated plexus of the trachga of the mouse (Chiang and Gabella, 1986), but there can be as many as 4000 neurons in the ferret (Baker et al., 1986).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 16.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Baker, D. G., Basbaum, C. B., Herbert, D. A., and Mitchell, R. A., 1983, Transmission in airway ganglia of ferrets: Inhibition by norepinephrine, Neurosci. Lett. 41: 139–143.

    Article  PubMed  CAS  Google Scholar 

  • Baker, D. G., McDonald, D. M., Basbaum, C. B., and Mitchell, R. A., 1986, The architecture of nerves and ganglia of the ferret trachea as revealed by acetylcholinesterasehistochemistry, J. Comp. Neurol. 246: 513–526.

    Article  PubMed  CAS  Google Scholar 

  • Bartlett, D., Jr., Jefferey, P., Sant’Ambrogio, G., and Wise, J. C. M., 1976, Location of stretch receptors in the trachea and bronchi of the dog,, J. Physiol. (Lond.) 258: 409–420.

    PubMed  Google Scholar 

  • Basbaum, C. B., Grillo, M. A., and Widdicombe, J. H., 1984, Muscarinic receptors: Evidence for a nonuniform distribution in tracheal smooth muscle and exocrine glands, J. Neurosci. 4: 508–520.

    PubMed  CAS  Google Scholar 

  • Blackman, J. G., and McCraig, D. J., 1982, Studies on an isolated innervated preparation of guinea-pig trachea, Br. J. Pharmacol. 80: 703–710.

    Google Scholar 

  • Bock, P., and Stockinger, L., 1984, Light and electron microscopic identification of elastic, elaunin and oxytalan fibers in human tracheal and bronchial mucosa, Anat. Embryol. 170: 145–153.

    Article  PubMed  CAS  Google Scholar 

  • Cadieux, A., Springall, D. R., Mulderry, P. K., Rodrigo, J., Ghatei, M. A., et al., 1986, Occurrence, distribution and ontogeny of CGRP immunoreactivity in the rat lower respiratory tract: Effect of capsaicin treatment and surgical denervations, Neuroscience 19: 605–627.

    Article  PubMed  CAS  Google Scholar 

  • Cameron, A. R., Bullock, C. G., and Kirkpatrick, C. T., 1982, Theultrastructure of bovine tracheal smooth muscle, J. Ultrastruct. Res. 81: 290–305.

    Article  PubMed  CAS  Google Scholar 

  • Cameron, A. R., Johnston, C. F., Kirkpatrick, C. T., and Kirkpatrick, M. C. A., 1983, The quest for the inhibitory neurotransmitter in bovine tracheal smooth muscle, Q. J. Exp. Physiol. 68: 413–426.

    CAS  Google Scholar 

  • Chesrown, S. E., Venugopalan, C. S., Gold, W. M., and Drazen, J. M., 1980, In vivo demonstration of nonadrenergic inhibitory innervation of the guinea pig trachea, J. Clin. Invest. 65: 314–320.

    Article  PubMed  CAS  Google Scholar 

  • Chian, C.-H., and Gabella, G., 1986, Quantitative study of the ganglion neurons of the mouse trachea, Cell Tissue Res. 100: 243–252.

    Article  Google Scholar 

  • Coburn, R. F., and Tomita, T., 1973, Evidence for noradrenergic inhibitory nerves in the guinea pig trachealis muscle, Am. J. Physiol. 224: 1072–1080.

    PubMed  CAS  Google Scholar 

  • Coleman, R. A., and Levy, G. P., 1974, A non-adrenergic inhibitory nervous pathway in guinea-pig trachea, Br. J. Pharmacol. 52: 167–174.

    PubMed  CAS  Google Scholar 

  • Dahlstrom, A., Fuxe, K., Hokfelt, T., and Norberg, K.-A., 1966, Adrenergic innervation of the bronchial muscle of the cat, Acta Physiol. Scand. 66: 507–508.

    Article  PubMed  CAS  Google Scholar 

  • Dalsgaard, C.-J., and Lundberg, J. M., 1984, Evidence for a spinal afferent innervation of the guinea pig lower respiratory tract as studied by the horseradish peroxidase technique, Neurosci. Lett. 45: 117–122.

    Article  PubMed  CAS  Google Scholar 

  • Daly, D. I., and Hebb, C, 1966, Pulmonary and Bronchial Vascular Systems, Edward Arnold, London.

    Google Scholar 

  • Daniel, E. E., Daniel, V. P., Duchon, G., Garfield, R. E., Nichols, M., Malhotra, S. K., and Oki, M., 1976, Is the nexus a necessary for cell-to-cell coupling in smooth muscle?,J. Membr. Biol. 208: 207–239.

    Google Scholar 

  • Daniel, E. E., Kannan, M., Davis, C, and Posey-Daniel, V., 1986, Ultrastructuralstudies on the neuromuscular control of human tracheal and bronchial muscle, Respir. Physiol. 63: 109–128.

    Article  PubMed  CAS  Google Scholar 

  • Dey, D. D., Shannon, W. A., and Said, S. I., 1981, Localization of VIP-immunoreactive nerves in airways and pulmonary vessels of dogs, cats, and human subjects, Cell Tissue Res. 220: 231–238.

    PubMed  CAS  Google Scholar 

  • Diamond, L., and O’Donnell, M., 1980, A nonadrenergic vagal inhibitory pathway to feline airways, Science 208: 185–188.

    Article  PubMed  CAS  Google Scholar 

  • During, M., Andres, K. H. and Iravani, J., 1974, The fine structure of the pulmonary stretch receptor in the rat, Z. Anat. Entwicklungsgesch. 143: 215–222.

    Article  Google Scholar 

  • El-Bermani, A.-W., and Grant, M., 1975, Acetylcholinesterase-positive nerves of the rhesus monkey bronchial tree, Thorax 30: 162–170.

    Article  PubMed  CAS  Google Scholar 

  • Fillenz, M., 1970, Innervation of pulmonary and bronchial blood vessels of the dog, J. Anat. (Lond.) 106: 449–461.

    PubMed  CAS  Google Scholar 

  • Fleisch, J. H., Maling, H. M., and Brodie, B. B., 1970, Evidence for existence of alpha-adrenergic receptors in the mammalian trachea, Am. J. Physiol. 218: 596–599.

    PubMed  CAS  Google Scholar 

  • Foster, R. W., 1964, A note on the electrically transmurally stimulated isolated trachea of the guinea-pig, J. Pharm. Pharmacol. 16: 125–128.

    Article  PubMed  CAS  Google Scholar 

  • Foster, R. W., and O’Donnell, S. R., 1972, Some evidence of the active uptake of noradrenaline in the guinea-pig isolated trachea, Br. J. Pharmacol. 45: 71–82.

    PubMed  CAS  Google Scholar 

  • Gabella, G., 1981, Structure of smooth muscles, in: Smooth Muscle: An Assessment of Current Knowledge (E. BĂĽlbring, A. F. Brading, A. W. Jones, and T. Tomita, eds.), pp. 1–46, Edward Arnold, London.

    Google Scholar 

  • Holmes, R., and Torrance, R. W., 1959, Afferentfibres of the stellate ganglion, Q. J. Exp. Physiol. 44: 271–281.

    CAS  Google Scholar 

  • Hoyes, A. D., and Barber, P., 1980, Innervation of the trachealis muscle in the guinea-pig: A quantitativeultrastructuralstudy, J. Anat. (Lond.) 130: 789–800.

    PubMed  CAS  Google Scholar 

  • Irvin, C. G., Boileau, R., Tremblay, J., Martin, R. R., and Macklem, P. T., 1980, Bronchodilatation: Noncholinergic, nonadrenergic mediation demonstrated in vivo in the cat, Science 207: 791–792.

    Article  PubMed  CAS  Google Scholar 

  • Jacobowitz, D., Kent, K. M., Fleisch, J. H., and Cooper, T., 1973, Histofluorescence study of catecholamine-containing elements in cholinergic ganglia from the calf and dog lung, Proc. Soc. Exp. Biol. Med. 144: 464–466.

    PubMed  CAS  Google Scholar 

  • Jones, T. R., Kannan, M. S., and Daniel, E. E., 1980, Ultrastructuralstudy of guinea pig tracheal smooth muscle and its innervation, Can. J. Physiol. Pharmacol. 58: 974–983.

    Article  PubMed  CAS  Google Scholar 

  • Kalia, M., Cameron, A. R., and Coburn, R. F., 1983, Morphological characteristics of physiologically identified parasympathetic nerve fibers in ferret trachealis muscle, Fed. Proc. 42: 999.

    Google Scholar 

  • Kannan, M. S., and Daniel, E. E., 1980, Structural and functional study of canine tracheal smooth muscle, Am. J. Physiol. 238: C27–C33.

    PubMed  CAS  Google Scholar 

  • Kneussl, M. P., and Richardson, J. P., 1978, Alpha-adrenergic receptors in human and canine tracheal and bronchial smooth muscle, J. Appl. Physiol. 45: 307–311.

    PubMed  Google Scholar 

  • Knight, D. S., 1980, A light and electron microscopic study of feline intrapulmonary ganglia, J. Anat. (Lond.) 131: 413–428.

    CAS  Google Scholar 

  • Knight, D. S., Hyman, A. L., and Kadowitz, P. J., 1981, Innervation of intrapulmonary airway smooth muscle of the dog, monkey and baboon, J. Auton. Nerv. Syst. 3: 31–43.

    Article  PubMed  CAS  Google Scholar 

  • Laitinen, A., 1985, Autonomic innervation of the human respiratory tract as revealed by histochemical and ultrastructuralmethods, Eur. J. Respir.Dis. (suppl. 140) 66: 1–42.

    Google Scholar 

  • Lundberg, J. M., and Saria, A., 1982, Bronchial smooth muscle contraction induced by stimulation of capsaicin-sensitive sensory neurons, Acta Physiol. Scand. 116: 473–476.

    Article  PubMed  CAS  Google Scholar 

  • Lundberg, J. M., and Saria, A., 1987, Polypeptide-containing neurons in airway smooth muscle, Annu. Rev. Physiol. 49: 557–572.

    Article  PubMed  CAS  Google Scholar 

  • Lundberg, J. M., Martling, C.-R., and Saria, A. 1983, Substance P and capsaicin-induced contraction of human bronchi, Acta Physiol. Scand. 119: 49–53.

    Article  PubMed  CAS  Google Scholar 

  • Lundberg, J. M., Brodin, E., Hua, X., and Saria, A., 1984a, Vascular permeability changes and smooth muscle contraction in relation to capsaicin-sensitive substance P affĂ©rents in the guinea-pig, Acta Physiol. Scand. 120: 217–227.

    Article  PubMed  CAS  Google Scholar 

  • Lundberg, J. M., Hokfelt, T., Martling, C. R., Saria, A., and Cuello, C, 1984b, Substance P-immunoreactive sensory nerves in the lower respiratory tract of various mammals including man, Cell Tissue Res. 235: 251–261.

    Article  PubMed  CAS  Google Scholar 

  • Mann, S. P., 1971, The innervation of mammalian bronchial smooth muscle: The localization of catecholamines and cholinesterases, Histochem. J. 3: 319–331.

    Article  PubMed  CAS  Google Scholar 

  • Matsuzaki, Y., Hamasaki, Y., and Said, S. I., 1980, Vasocactive intestinal peptide: A possible transmitter of adrenergic relaxation of guinea pig airways, Science 210: 1252–1253.

    Article  PubMed  CAS  Google Scholar 

  • Mortola, J. P., and Sant ’Ambrogio, G., 1979, Mechanics of the trachea and behaviour of its slowly adapting stretch receptors, J. Physiol. (Lond.) 286: 577–590.

    CAS  Google Scholar 

  • Mustafa, K. Y., Elkhawad, A. O., Bicik, V., Mardini, I. A., and Thulesius, O., 1982, Adrenergic and cholinergic induced contractions of tracheal smooth muscle in the rabbit as demonstrated by a new in vivo methods, Acta Physiol. Scand. 114: 129–134.

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell, S. R., and Saar, N., 1973, Histochemical localization of adrenergic nerves in the guinea-pig trachea, Br. J. Pharmacol. 47: 707–710.

    PubMed  Google Scholar 

  • O’Donnell, S. R., Saar, N., and Wood, L. J., 1978, The density of adrenergic nerves at various levels in the guinea-pig lung, Clin. Exp. Pharmacol. Physiol. 5: 325–332.

    Article  PubMed  Google Scholar 

  • Pack, R. J., Al-Ugaily, L. H., and Widdicombe, J. G., 1984, The innervation of the trachea and extrapulmonary bronchi of the mouse, Cell Tissue Res. 338: 61–68.

    Google Scholar 

  • Pack, R. J., and Richardson, P. S., 1984, Theaminergic innervation of the human bronchus: A light and electron microscopic study, J. Anat. (Lond.) 138: 493–502.

    Google Scholar 

  • Richardson, J., and Beland, J., 1976, Nonadrenergic inhibitory nervous system in human airways, J. Appl. Physiol. 41: 164–11.

    Google Scholar 

  • Richardson, J. B., and Ferguson, C. C, 1979, Neuromuscular structure and function in the airways, Fed. Proc. 38: 202–208.

    PubMed  CAS  Google Scholar 

  • Sant ’Ambrogio, G., 1982, Information arising from the tracheobronchial tree of mammals, Physiol. Rev. 62: 531–569.

    Google Scholar 

  • Sheppard, M. N., Kurian, S. S., Henzen-Longmans, S. C, Michetti, F., Cocchia, D., Cole, P., Rush, R. A., Marangos, P. J., Bloom, S. R., and Polak, J. M., 1983, Neurone-specific enolase and S-100: New markers for delineating the innervation of the respiratory tract in man and other mammals, Thorax 38: 333–340.

    Article  PubMed  CAS  Google Scholar 

  • Silva, D. G., and Ross, G., 1974, Ultrastructuraland fluorescence histochemical studies on the innervation of the tracheo bronchial muscle of normal cats and cats treated with 6-hydroxydopamine, J. Ultrastruc. Res. 47:310–328.

    Article  CAS  Google Scholar 

  • Smith, R. V., and Satchell, D. G., 1985, Extrinsic pathways of the adrenergic innervation of the guinea-pigtrachealis muscle, J. Auton. Nerv. Syst. 14:61–73.

    Article  PubMed  CAS  Google Scholar 

  • Smith, R. V., and Taylor, I. M., 1971, Observations on the intrinsic innervation of trachea, bronchi and pulmonary vessels in the sheep, Acta Anat. 80:1–13.

    Article  PubMed  CAS  Google Scholar 

  • Suzuki, H., Morita, K., and Kuriyama, H., 1976, Innervation and properties of the smooth muscle of the dog trachea, Jpn. J. Physiol. 26: 303–320.

    Article  PubMed  CAS  Google Scholar 

  • Szolcsanyi, J., and Bartho, L., 1982, Capsaicin-sensitive non-cholinergic excitatory innervation of the guinea-pig tracheobronchial smooth muscle, Neurosci. Lett. 34: 247–251.

    Article  PubMed  CAS  Google Scholar 

  • Uddman, R., Alumets, J., Densert, O., Hakanson, R., and Sundler, F., 1978, Occurrence and distribution of VIP nerves in the nasal mucosa and tracheobronchial wall, Acta. Otolaryngol. (Stockh.) 86: 443–448.

    CAS  Google Scholar 

  • Vornanen, M., 1982, Adrenergic responses in different sections of rat airways, Acta Physiol. Scand. 114: 587–591.

    Article  PubMed  CAS  Google Scholar 

  • Wailoo, M., and Emery, J. L., 1980, Structure of the membranous trachea in children, Acta Anat. (Basel) 106: 254–261.

    Article  PubMed  CAS  Google Scholar 

  • Widdicombe, J. G., 1954, Receptors in the trachea and bronchi of the cat, J. Physiol. (Lond.) 123: 71–104.

    CAS  Google Scholar 

  • Widdicombe, J. G., 1963, Regulation of tracheobronchial smooth muscle, Physiol. Rev. 43: 1–37.

    PubMed  CAS  Google Scholar 

  • Yip, Palomini, B., and Coburn, R. F., 1981, Inhibitory innervation to the guinea pig trachealis muscle, J. Appl. Physiol. 50: 374–382.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1989 Plenum Press, New York

About this chapter

Cite this chapter

Gabella, G. (1989). Structure of Airway Smooth Muscle and Its Innervation. In: Coburn, R.F. (eds) Airway Smooth Muscle in Health and Disease. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0779-2_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-4613-0779-2_1

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-8078-1

  • Online ISBN: 978-1-4613-0779-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics