Integration of Neural Inputs in Peripheral Airway Ganglia

  • Ronald F. Coburn


The goal of this chapter is to review information related to neural control of airway smooth muscle, and integration of neural inputs to airway smooth muscle. Neural inputs to airway smooth muscle can be controlled and modulated at the level of the central nervous system (CNS), the peripheral airway ganglia, and at the neuromuscular junction. Mechanisms of integration of neural inputs at the level of the peripheral airway parasympathetic ganglia and at the neuromuscular junction are discussed. Control and modulation at the level of the CNS are not discussed.


Vasoactive Intestinal Peptide Airway Smooth Muscle Postsynaptic Neuron Command Neuron Neural Input 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Akasu, T., Hirai, K., and Koketsu, K., 1981a, 5-Hydroxytryptamine controls ACh-receptor sensitivity of bullfrog sympathetic ganglion cells, Brain Res. 212: 217–220.CrossRefGoogle Scholar
  2. Akasu, T., Hirai, K., and Koketsu, K., 1981b, Increase of acetylcholine-receptor sensitivity by adnosine triphosphate: A novel action of ATP on ACh-sensitivity, Br. J. Pharmacol. 74:505–507.PubMedGoogle Scholar
  3. Altier, R. J., and Diamond, L., 1985, Effect of alpha chymotrypsin on the non-adrenergic, non-cholinergic inhibitory system in cat airways, Eur. J. Pharmacol. 114:75–78.CrossRefGoogle Scholar
  4. Altier, R. J., and Diamond, L., 1986, Role of vagal sensory fibers in nonadrenergicnoncholinergic inhibitory responses in cat airways, Am. Rev. Respir. Dis. 133:1159–1162.Google Scholar
  5. Altier, R. J., Szarek, J. L., and Diamond, L., 1984, Neural control of relaxations in cat airway smooth muscle, J. Appl. Physiol. . 57:1536–1548.Google Scholar
  6. Andersson, R. G., and Grundstrom, N., 1983, The excitatory non-cholinergic non-adrenergic nervous system of the guinea-pig airways, Eur. J. Respir. Dis. 131(Suppl.):141–157.Google Scholar
  7. Ashe, J. H., and Libit, B., 1981, Modulation of slow postsynaptic potentials by dopamine in rabbit sympathetic ganglion, Brain Res. 217:93–106.PubMedCrossRefGoogle Scholar
  8. 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.PubMedCrossRefGoogle Scholar
  9. 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.PubMedCrossRefGoogle Scholar
  10. Baluk, P., Fumiwara, T., and Martsuda, S., 1985, The fine structure of the ganglia of the guinea pig trachea, Cell Tissue Res. 239:51–60.PubMedCrossRefGoogle Scholar
  11. Blackman, J. G., Crawcroft, P. J., Devine, C. E., Holman, M. E., and Yonemura, K., 1969, Transmission from preganglionic fibres in the hypogastric nerve to peripheral ganglia of male guinea pigs, J. Physiol. (Lond.) 201:723–743.PubMedGoogle Scholar
  12. Bloomquist, E. I., and Kream, R. M., 1988, Leukotriene D4 acts in part to control guinea pig ileum smooth muscle by releasing substance P, J. Pharmacol. Exp. Ther. 240:523–528.Google Scholar
  13. Boyle, J. P., Davies, J. M., Foster, R. W., Morgan, G. W., and Small, R. C, 1987, Inhibitoryresponses to nicotine and transmural stimulation in hyoscine-treated guinea-pig isolated trachealis muscle, Br. J. Pharmacol. 90:733–744PubMedGoogle Scholar
  14. Cabezas, G. A., Graf, P. D., and Nadel, J., 1971, Sympathetic versus parasympathetic nervousregulation of airways in dogs, J. Appl. Physiol. 31:651–665.PubMedGoogle Scholar
  15. Cameron, A. R., and Coburn, R. F., 1981, Electrical properties of the cells of the ferret paratrachealganglion, Physiologist 24:84.Google Scholar
  16. Cameron, A. R., and Coburn, R. F., 1984, Electrical and anatomic characteristics of cells of theferret paratracheal ganglion, Am. J. Physiol. 246:C450–458PubMedGoogle Scholar
  17. Cameron, A. R., and Kirkpatrick, C. T., 1977, A study of excitatory neuromuscular transmission inthe bovine trachea, J. Physiol. (Lond.) 270:733–745.Google Scholar
  18. Cameron, A. R., Bullock, C. G., and Kirkpatrick, C. T. 1982, The ultrastructure of bovine trachealsmooth muscle, J. Ultrastruct. Res. 81:290–305.PubMedCrossRefGoogle Scholar
  19. Cameron, A. R., Johnston, C. F., Kirkpatrick, C. T., and Kirkpatrick, M. C. A., 1983, The questfor the inhibitory neurotransmitter in bovine tracheal smooth muscle, Q. J. Exp. Physiol. 68:413–426.PubMedGoogle Scholar
  20. Chiang, C. H., and Gabella, G., 1986, Quantitative study of the ganglion neurons of the mousetrachea, Cell Tissue 100:243–252.CrossRefGoogle Scholar
  21. 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. 654:315–320.Google Scholar
  22. Christ, D. D., and Nishi, S., 1969, Presynaptic action of epinephrine on sympathetic ganglia, Life Sci. 8:1235–1238PubMedCrossRefGoogle Scholar
  23. Chung, K. F., Evans, T. W., Graf, P. D., and Nadel, J. A., 1985, Modulation of cholinergicneurotransmission in canine trachealis muscle by thromboxane mimetic U46619, Br. J. Pharmacol. 117:373–375.Google Scholar
  24. Coburn, R. F., 1984a, Neural coordination of excitation of ferret trachealis muscle, Am. J. Physiol. 246:C459–466.PubMedGoogle Scholar
  25. Coburn, R. F., 1984b, The anatomy of the ferret paratracheal parasympathetic nerve-ganglionplexus, Exp. Lung Res. 7:1–9.PubMedCrossRefGoogle Scholar
  26. Coburn, R. F., 1987, Colinergicneuroeffector mechanisms in airway smooth muscle, in: TheAirways, Neural Control in Health and Disease, Vol. 33: Lung Biology in Health and Disease,M. A. Kaliner and P. T. Barnes, eds.), pp. 159–186, Marcel Dekker, New York.Google Scholar
  27. Coburn, R. F., and Kalia, M. P., 1986, Morphological features of spiking and nonspiking cells in theparatracheal ganglion of the ferret, J. Comp. Neurol. 254:341–351.PubMedCrossRefGoogle Scholar
  28. Coburn, R. F., and Tomita, T., 1973, Evidence for nonadrenergic inhibitory nerves in the guinea pigtrachealis muscle, Am. J. Physiol. 224:1072–1080.PubMedGoogle Scholar
  29. Coburn, R. F., 1987, Effect of norepinephrine on neurotransmission in the AH cell of the ferretparatracheal ganglion, Fed. Proc. 46:704.Google Scholar
  30. Coleman, R. A., and Levy, G. P., 1974, A non-adrenergic inhibitory nervous pathway in the guineapig trachea, Br. J. Pharmacol. 52:167–174.PubMedGoogle Scholar
  31. Dahlstrom, A., Fuxe, K., Hokfelt, T., and Norberg, K. A., 1966, Adrenergic innervation of thebronchial muscle of the cat, Acta Physiol. Scand. 66:507–508.PubMedCrossRefGoogle Scholar
  32. DeGroat, W. C, and Booth, A. M., 1980, Inhibition and facilitation in parasympathetic ganglia ofthe urinary bladder, Fed. Proc. 39:2990–2996.Google Scholar
  33. DeGroat, W. C, and Saum, W. A., 1971, Adrenergic inhibition in mammalian parasympatheticganglia, Nature New Biol. 231:188–189.CrossRefGoogle Scholar
  34. Dey, R. D., Shannon, J.W.A., and Said, S. A., 1981, Localization of VIP immunoreactive nerves inairway and pulmonary vessels of dogs, cats and human subjects, Cell Tissue Res. 222:231–239.Google Scholar
  35. Diamond, L., and O’Donnell, M., 1980, A nonadrenergic vagal inhibitory pathway in feline airways, Science 208:185–188.PubMedCrossRefGoogle Scholar
  36. Eranko, O., and Harkonen, M., 1963, Histochemical demonstration of fluorgenic amines in thecytoplasm of sympathetic ganglion cells of the rat, Acta Physiol. 58:285–286.CrossRefGoogle Scholar
  37. Fowler, J. C, and Weinreich, D., 1986, Electrophysiological membrane properties of paratrachealganglion neurons of the rabbit, Neurosci.Abstr. 11:1182.Google Scholar
  38. Fryer, A. D., and Maclagan, J., 1984, Muscarinic inhibitory receptors in pulmonary parasympatheticnerves in the guinea pig, Br. J. Pharmacol. 83:973–978.PubMedGoogle Scholar
  39. Gaban, M., and Adams, P. R., 1982, Control of calcium current in rat sympathetic neurons bynorepinephrine, Brain Res. 244:155–144.CrossRefGoogle Scholar
  40. Gallagher, J. P., Griffith, W. J., III, and Shinnick-Gallagher, P., 1982, Cholinergic transmission incat parasympathetic neurons, J. Physiol. (Lond.) 332:473–486.Google Scholar
  41. Goyal, R. K., Rattan, S., and Said, S. I., 1980, VIP as a possible neurotransmitter of noncholinergic, non-adrenergic inhibitory neurones, Nature (Lond.) 288:378–380.CrossRefGoogle Scholar
  42. Greene, J. H., and Coburn, R. F., 1988, VIP and the inhibitory neurotransmitter in the guinea pigtrachealis muscle (submitted)Google Scholar
  43. Griffith, W. H. III, Gallagher, J. P., and Shinnick-Gallagher, P., 1981a, Sucrose-gap recordings ofnerve-evoked potentials in mammalian parasympathetic ganglia, Brain Res. 209:446–451.PubMedCrossRefGoogle Scholar
  44. Griffith, W. H. III, Gallagher, J. P., and Shinnick-Gallagher, P., 1981b, Mammalian parasympathetic ganglia fire spontaneous action potentials and transmit slow potentials, in: Advances inPhysiological Sciences Vol 4. Physiology of Excitable Membranes (J. Salanki, ed.), pp. 347–350, AdademialKiado, Budapest.Google Scholar
  45. Inoue, T., and Ito, Y., 1985, Pre- and post-junctional effects of prostaglandin I2 and leukotriene C4in dog tracheal tissue. Br. J. Pharmacol. 84:289–298.PubMedGoogle Scholar
  46. Inoue, T., Ito, Y., and Takeda, K., 1984, Prostaglandin induced inhibition of acetylcholine releasefrom neuronal elements of dog tracheal tissue, J. Physiol. (Lond.) 349:553–570.Google Scholar
  47. Jacobowitz, D., Kent, K. M., Fleisch, J. H., and Cooper, T., 1973, Histofluorescent study ofcatecholamine-containing elements in cholinergic ganglion from the calf and dog lung, Proc.Soc. Exp. Biol. Med. 144:464–466.PubMedGoogle Scholar
  48. Karczmar, A. G., Koketsu, K., and Nishi, S., 1986, Autonomic and Enteric Ganglia, Plenum, NewYork.Google Scholar
  49. Kawatani, M., Rutigliano, M., and DeGroat, W. C, 1986, Selective facilitatory effects of vasoactive intestinal polypeptide on muscarinic mechanisms in sympathetic and parasympatheticganglia of the cat, in: Dynamics of Cholinergic Function, (I. Hanin, ed.), Plenum, NewYork.Google Scholar
  50. Knight, D. S., 1980, A light and electron microscopic study of feline intrapulmonary ganglia, J.Anat. (Lond.) 131:413–428.Google Scholar
  51. Knight, D. S., Hyman, A. L., and Kadowitz, P. J., 1981, Innervation of intrapulmonary airwaysmooth muscle of the dog, monkey and baboon, J. Auton. Nerv. Syst. 3:31–43.PubMedCrossRefGoogle Scholar
  52. Koketsu, K., 1981, Electropharmacological actions of catecholamine in sympathetic ganglia: Multiple modes of actions to modulate the nicotinic transmission, Jpn. J. Pharmacol. 31(Suppl.):27P–28P.PubMedGoogle Scholar
  53. Koketsu, K., and Minota, S., 1975, The direct action of adrenaline on the action potentials ofbullfrog’s sympathetic ganglion cells, Experientia 31:822–823.PubMedCrossRefGoogle Scholar
  54. Laitinen, A., Partanen, M., Hervonen, A., and Laitinen, L. A., 1985, Electron microscopic study on the innervation of the human lower respiratory tract: Evidence of adrenergic nerves, Eur. J.Respir. Dis. 67:209–215.PubMedGoogle Scholar
  55. Leff, A. R., Munoz, N. M., and Hendrix, S. G., 1983, Parasympathetic and adrenergic contractileresponses in canine trachea and bronchus, J. Appl. Physiol. 55:113–120.PubMedGoogle Scholar
  56. Lichtman, J. W., 1980, On the predominantly single innervation of submandibular ganglion cells inthe rat, J. Physiol. (Lond.) 302:121–130.Google Scholar
  57. Lichtman, J. W., Purves, D., and Yip, J. W., 1979, On the purpose of selective innervation ofguinea-pig superior cervical ganglion cells,J. Physiol. (Lond.) 292:69–84.Google Scholar
  58. Lundberg, J. M., and Hokfelt, T., 1983, Coexistence of peptides and classification of neurotransmitters, Trends Neurosci.6:325–333.CrossRefGoogle Scholar
  59. Lundberg, J. M., and Sana, A., 1982, Bronchial smooth muscle contraction induced by stimulation of capsaicin-sensitive sensory neurons, Acta Physiol. Scand. 116:473–476.PubMedCrossRefGoogle Scholar
  60. Lundberg, j. M., Sana, A., Brodin, E., Rosell, S., and Folkers, K., 1983, A substance P antagonist inhibits vagally induced increase in vascular permeability and bronchial smooth muscle contraction of the guinea pig, Proc. Natl. Acad. Sci. USA 80:1120–1124.PubMedCrossRefGoogle Scholar
  61. Mann, S., 1971, The innervation of mammalian bronchial smooth muscle: The localization of catecholamines and cholinesterases, Histochem. J. 3:319–331.PubMedCrossRefGoogle Scholar
  62. Matsuzaki, Y., Hamasaki, Y., and Said, S. I., 1980, Vasoactive intestinal peptide: A possible transmitter of nonadrenergic relaxation of guinea pig airways, Science 210:1252–1253.PubMedCrossRefGoogle Scholar
  63. Middendorf, W. F., and Russell, J. A., 1980, Innervation of airway smooth muscle in the baboon. Evidence for a nonadrenergic inhibitory system, J. Appl. Physiol. 48:947–956.PubMedGoogle Scholar
  64. Minette, P. A., and Barnes, P. J., 1988, Prejunctional inhibitory muscarinic receptors on cholinergic nerves in human and guinea pig airways, J. Appl. Physiol. 64:2532–2537.PubMedGoogle Scholar
  65. Mitchell, R. A., Herbert, D. A., Baker, D. G., and Basbaum, C. B., 1987, In vivo activity of tracheal parasympathetic ganglion cells innervating tracheal smooth muscle, Brain Res. 437: 157–160.PubMedCrossRefGoogle Scholar
  66. Nishi, S., and Christ, D. D., 1971, Electrophysiological and anatomical properties of mammalian parasympathetic ganglion cells, in: Proceedings of the International Union of Physiological Sciences, Vol. 9, pp. 421–431, German Physiological Society, Munich.Google Scholar
  67. North, R. A., 1973, The calcium-dependent slow after hyperpolarization in myenteric neurons with TTX-resistant action potentials, Br. J. Pharmacol. 49:709–711.PubMedGoogle Scholar
  68. O’Donnell, S. R., and Saar, N., 1973, Histochemical localization of adrenergic nerves in the guinea pig trachea, Br. J. Pharmacol. 47:707–710.PubMedGoogle Scholar
  69. Ohta, Y., and Koketsu, K., 1984, Histamine as an endogenous antagonist of nicotinic Ach-receptor, Brain Res. 306:370–373.PubMedCrossRefGoogle Scholar
  70. Pennefather, P., Lancaster, B., Adams, P. R., and Nicoll, R. A., 1985, Two distinct Ca-dependent K currents in bullfrog sympathetic ganglion cell, Proc. Nat. Acad. Sci. USA 82:3040–3042.PubMedCrossRefGoogle Scholar
  71. Purves, D., and Wigston, D. J., 1983, Neural units in the superior cervical ganglion of the guinea-pig, J. Physiol. (Lond.) 334:169–178.Google Scholar
  72. Richardson, J., and Beland, J., 1976, Nonadrenergic inhibitory nerves in human airways, J. Appl. Physiol. 41:764–771.PubMedGoogle Scholar
  73. Russell, J. A., 1978, Responses of isolated canine airways to electrical stimulation and acetylcholine, J. Appl. Physiol. 45:690–698.PubMedGoogle Scholar
  74. Russell, J. A., and Bartlett, J., 1981, Adrenergic neurotransmission in airways: Inhibition by acetylcholine, J. Appl. Physiol. 52:376–383.CrossRefGoogle Scholar
  75. Russell, J. A., and Simon, E. J., 1985, Modulation of cholinergic neurotransmission in airways by enkephalin, J. Appl. Physiol. 58:853–858.PubMedGoogle Scholar
  76. Seria, R., and Daniel, E. E., 1988, Thromboxane effect on canine trachealis neuromuscular function, J. Appl. Physiol. 64:1979–1988.Google Scholar
  77. Sheller, J. R., Holtzman, J. J., Skoogh, B. E., and Nadel, J. A., 1982, Interaction of serotonin with vagal and acetylcholine induced bronchoconstriction in canine lungs, J. Appl. Physiol. 52:964–966.PubMedGoogle Scholar
  78. Simonds, W. F., Booth, A. M., Thor, K. B., Ostrowski, N. L., Nagel, J. R., and DeGroat, W. C, 1983, Parasympathetic ganglia: Naloxone antagonizes inhibition by leucine-enkephalin and GABA, Brain Res. 271:365–370.PubMedCrossRefGoogle Scholar
  79. Skoogh, B. E., 1986, Transmission through airways ganglia, Eur. J. Respir. Dis. 131(Suppl.):159–170.Google Scholar
  80. Suzuki, T., and Kusano, K., 1978, Hyperpolarizing potentials induced by Ca-mediated K conduction increase in hamster submandibular ganglion cells, J. Neurobiol. 9:367–392.PubMedCrossRefGoogle Scholar
  81. Tamura, K., Palmer, J. M., and Wood, J. D., 1988, Presynaptic inhibition produced by histamine atnicotinic synapses in enteric ganglia, Neurosci.25:171–179.CrossRefGoogle Scholar
  82. Tanaka, D. T., and Grunstein, M. D., 1984, Mechanisms of substance P-induced contraction ofrabbit airway smooth muscle, J. Appl. Physiol. 57:1551–1557.PubMedGoogle Scholar
  83. Uddman, R. J., Aluments, J., Senset, O., Hakanson, R., and Sundler, F., 1978, Occurrence anddistribution of VIP nerves in the nasal mucosa and tracheal-bronchial wall, ActaOtolaryngol.(Stockh.) 86:433–448.Google Scholar
  84. Vanhoutte, P. M., Verbeurent, J., and Webb, R. C, 1981, Local modulation of adrenergic neuroeffector interactions in the blood vessel wall, Physiol. Rev. 61:151–247.PubMedGoogle Scholar
  85. Walters, E. H., O’Bryne, P. M., Fabbri, L. M., Graf, P. D., Holtzman, M. J., and Nadel, J. A.,1984, Control of neurotransmission by prostaglandins in canine tracheaiis smooth muscle, J.Appl. Physiol. 57:128–134.Google Scholar
  86. Wood, J. D., 1984, Enteric neurophysiology, Am. J. Physiol. 247:G585–598.PubMedGoogle Scholar
  87. Yip, P., Palombini, B., and Coburn, R. F., 1981, Inhibitory innervation to the guinea pig tracheaiismuscle, J. Appl. Physiol. 50:374–382.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1989

Authors and Affiliations

  • Ronald F. Coburn
    • 1
  1. 1.Department of PhysiologyUniversity of Pennsylvania School of MedicinePhiladelphiaUSA

Personalised recommendations