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Afferent Innervation of the Esophagus in Cat and Rat

  • Winfried L. Neuhuber
  • Nadine Clerc

Abstract

Afferent neurons connecting the gastrointestinal tract with the brainstem and spinal cord are important for regulation and coordination of the various motor, absorptive and secretory functions of this organ system. Thus, afferent signals and feedback are as much important for, e.g., an orderly progression of swallowing (Falempin et al., 1986) as they are for defecation and continence (for reviews see Christensen, 1987; Gonella et al., 1987). Other gastrointestinal functions are also more or less dependent on, or influenced by, afferent information (for reviews see Mei, 1983, 1985; Roman and Gonella, 1987). Visceroafferent neurons not only transmit information from the periphery to the central nervous system, but seem to be involved also in local “effector” actions in various organs (for reviews see Dockray and Sharkey, 1986; Holzer et al., 1987; Maggi and Meli, 1988).

Keywords

Dorsal Root Ganglion Neuron Enteric Neuron Myenteric Ganglion Circular Muscle Layer Nodose Ganglion 
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.

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References

  1. Aldskogius, H., Elfvin, L.-G., and Andersson Forsman, C., 1986, Primary sensory afferents in the inferior mesenteric ganglion and related nerves of the guinea pig, J. Autonom. Nerv. Syst., 15:179–190CrossRefGoogle Scholar
  2. Altschuler, S. M., Bao, X., Bieger, D., Hopkins, D. A., and Miselis, R. R., 1989, Viscerotopic representation of the upper alimentary tract in the rat: Sensory ganglia and nuclei of the solitary and spinal trigeminal tracts, J. Comp. Neurol., 283:248–268PubMedCrossRefGoogle Scholar
  3. Andres, K. H., 1966, Ueber die Feinstruktur der Rezeptoren an Sinushaaren, Z. Zellforscfh., 75:339–365CrossRefGoogle Scholar
  4. Andres, K. H., Düring, M. von, and Schmidt, R. F., 1985, Sensory innervation of the Achilles tendon by group III and IV afferent fibers, Anat. Embryol., 172:145–156PubMedCrossRefGoogle Scholar
  5. Andrew, B. L., 1956, The nervous control of the cervical oesophagus of the rat during swallowing, J. Physiol. (Lond.), 134:729–740Google Scholar
  6. Andrew, B. L., 1957, Activity in afferent nerve fibers from the cervical oesophagus, J. Physiol. (Lond.), 135:54–55PGoogle Scholar
  7. Andrews, P. L. R., 1986, Vagal afferent innervation of the gastrointestinal tract, in: “Visceral Sensation, Progress in Brain Research, Vol. 67,” F. Cervero and J. F. B. Morrison, eds., Elsevier, Amsterdam: 65–86Google Scholar
  8. Andrews, P. L. R., Grundy, D., and Scratchend, T., 1980, Vagal afferent discharge from mechanoreceptors in different regions of the ferret stomach, J. Physiol. (Lond.), 298:513–524Google Scholar
  9. Andrews, P. L. R., and Lang, K. M., 1982, Vagal afferent discharge from mechanoreceptors in the lower oesophagus of the ferret, J. Physiol. (Lond.), 332:29PGoogle Scholar
  10. Benedeczky, I., and Halasy, K., 1988, Visualization of non-synaptic release sites in the myenteric plexus of the snail Helix pomatia, Neuroscience, 25:163–170CrossRefGoogle Scholar
  11. Bower, A.J., and Parry, K., 1978, A demonstration of the use of autoradiography as a method of exploring afferent autonomic innervation of the respiratory tract, J. Physiol. (Lond.), 281:3–4PGoogle Scholar
  12. Böck, P., and Gorgas, K., 1976, Fine structure of baroreceptor terminals in the carotid sinus of guinea pigs and mice, Cell. Tiss. Res., 170:95–112CrossRefGoogle Scholar
  13. Brettschneider, H., 1966, Ultrastruktur der visceralen Rezeptoren und afferenten Nerven, Acta neuroveget., 28:37–102CrossRefGoogle Scholar
  14. Chambers, M.R., Andres, K. H., Düring, M. von, and Iggo, A, 1972, Structure and function of the slowly adapting type II mechanoreceptor in hairy skin, Quart J. Exp. Physiol., 57:417–445PubMedGoogle Scholar
  15. Christensen, J., 1987, Motility of the colon, in: “Physiology of the Gastrointestinal Tract, 2nd Ed.,” L. R. Johnson, ed., Raven Press, New York: 665–693Google Scholar
  16. Christensen, J., Rick, G. A., and Soll, D. J., 1987, Intramural nerves and interstitial cells revealed by the Champy-Maillet stain in the opossum esophagus, J. Autonom. Nerv. Syst., 19:137–151CrossRefGoogle Scholar
  17. Christensen, J., and Robison, G. A., 1985, Nerve cell density in submucous plexus throughout the gut of the cat and opossum, Gastroenterology, 89:1064–1069PubMedGoogle Scholar
  18. Clarke, G. D., and Davison, J. S., Tension receptors in the oesophagus and stomach of the rat, J. Physiol. (Lond.), 244:41–42PGoogle Scholar
  19. Clerc, N., 1983, Afferent innervation of the lower oesophageal sphincter of the cat. An HRP study, J. Autonom. Nerv. Syst., 9:623–636CrossRefGoogle Scholar
  20. Clerc, N., 1984, Afferent innervation of the lower oesophageal sphincter of the cat. Pathways and functional characteristics, J. Autonom. Nerv. Syst., 10:213–217CrossRefGoogle Scholar
  21. Clerc, N., and Condamin, M., 1987, Selective labeling of vagal sensory nerve fibers in the lower esophageal sphincter with anterogradely transported WGA-HRP, Brain Res., 424:216–224PubMedCrossRefGoogle Scholar
  22. Clerc, N., and Mei, N., 1983 a, Thoracic esophageal mechanoreceptors connected with fibers following sympathetic pathways, Brain Res. Bull., 10:1–7Google Scholar
  23. Clerc, N., and Mei, N., 1983 b, Vagal mechanoreceptors located in the lower oesophageal sphincter of the cat, J. Physiol. (Lond.), 336:487–498Google Scholar
  24. Delbro, D., 1985, The role of substance P in the control of gut motility, in: “Tachykinin Antagonists,” R. Hakanson and F. Sundler, eds., Elsevier, Amsterdam: 223–230Google Scholar
  25. Dockray, G. J., and Sharkey, K. A., 1986, Neurochemistry of visceral afferent neurones, in: “Visceral Sensation, Progress in Brain Research, Vol. 67,” F. Cervero and J. F. B. Morrison, eds., Elsevier, Amsterdam: 133–148CrossRefGoogle Scholar
  26. Düring, M. von, and Andres, K. H., 1969, Zur Feinstruktur der Muskelspindel von Mammalia, Anat. Anz., 124:566–573Google Scholar
  27. Düring, M. von, Andres, K. H., and Iravani, J., 1974, The fine structure of the pulmonary stretch receptor in the rat, Z. Anat. Entwickl.-Gesch., 143:215–222CrossRefGoogle Scholar
  28. El Ouazzani, T., and Mei, N., 1982, Electrophysiologic properties and role of the vagal thermoreceptors of lower esophagus and stomach in the cat, Gastroenterology, 83:995–1001PubMedGoogle Scholar
  29. Falempin, M., Madhloum, A., and Rousseau, J. P., 1986, Effects of vagal deafferentation on oesophageal motility and transit in the sheep, J. Physiol. (Lond.), 372:425–436Google Scholar
  30. Falempin, M., Mei, N., and Rousseau, J. P., 1978, Vagal mechanoreceptors of the inferior thoracic oesophagus, the lower oesophageal sphincter and the stomach in the sheep, Pflügers Arch., 373:25–30PubMedCrossRefGoogle Scholar
  31. Fryscak, T., Zenker, W., and Kantner, D., 1984, Afferent and efferent innervation of the rat esophagus. A tracing study with horseradish peroxidase and nuclear yellow, Anat. Embryol., 170:63–70PubMedCrossRefGoogle Scholar
  32. Gabella, G., 1972, Fine structure of the myenteric plexus in the guinea pig ileum, J. Anat., 111:69–97PubMedGoogle Scholar
  33. Gabella, G., and Trigg, P., 1984, Size of neurons and glial cells in the enteric ganglia of mice, guinea-pigs, rabbits and sheep, J. Neurocytol., 13:49–71PubMedCrossRefGoogle Scholar
  34. Gibbins, I. L., Furness, J. B., Costa, M., MacIntyre, I., Hillyard, C. J., and Girgis, S., 1985, Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs, Neurosci. Lett., 57:125–130PubMedCrossRefGoogle Scholar
  35. Gonella, J., Bouvier, M., and Blanquet, F., Extrinsic nervous control of motility of small and large intestines and related sphincters, Physiol. Rev., 67:902–962Google Scholar
  36. Green, T., and Dockray, G. J., 1988, Characterization of the peptidergic afferent innervation of the stomach in the rat, mouse and guinea-pig, Neuroscience, 25:181–193PubMedCrossRefGoogle Scholar
  37. Gruber, H., 1968, Ueber Struktur und Innervation der quergestreiften Muskulatur des Oesophagus der Ratte, Z. Zellforsch., 91:236–247PubMedCrossRefGoogle Scholar
  38. Halata, Z., 1988, Ruffini corpuscule — a stretch receptor in the connective tissue of the skin and locomotion apparatus, in: “Transduction and Cellular Mechanisms in Sensory Receptors, Progress in Brain Research, Vol. 74,” W. Hamann and A. Iggo, eds., Elsevier, Amsterdam: 221–229CrossRefGoogle Scholar
  39. Hamilton, D. W., 1968, The calyceal synapse of type I vestibular hair cells, J. Ultrastruct. Res., 23:98–114PubMedCrossRefGoogle Scholar
  40. Harding, R., and Titchen, D. A., 1975, Chemosensitive vagal endings in the esophagus of the cat, J. Physiol. (Lond.), 247:52–53PGoogle Scholar
  41. Holzer, P., 1988, Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides, Neuroscience, 24:739–768PubMedCrossRefGoogle Scholar
  42. Holzer, P., Schluet, W., Lippe, Th., and Sametz, W., 1987, Involvement of capsaicin-sensitive sensory neurons in gastrointestinal function, Acta Physiol. Hung., 69:403–411PubMedGoogle Scholar
  43. Ide, C., Yoshida, Y., Hayashi, S., Takashio, M., and Munger, B. L., 1988, A re-evaluation of the cytology of cat Pacinian corpuscules. II. The extreme tip of the axon, Cell. Tiss. Res., 253:95–103CrossRefGoogle Scholar
  44. Iggo, A., 1957, Gastro-intestinal tension receptors with unmyelinated afferent fibres in the vagus of the cat, Quart. J. Exp. Physiol., 42:130–141PubMedGoogle Scholar
  45. Iggo, A., and Andres, K. H., 1982, Morphology of cutaneous receptors, Ann. Rev. Neurosci., 5:1–31CrossRefGoogle Scholar
  46. Jänig, W., and Morrison, J. F. B., 1986, Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception, in: “Visceral Sensation, Progress in Brain Research, Vol. 67,” F. Cervero and J. F. B. Morrison, eds., Elsevier, Amsterdam: 87–114Google Scholar
  47. Kadanoff, D., 1966, Histologie visceraler Rezeptoren und visceral-afferenter Nerven, Acta neuroveget., 28:4–36CrossRefGoogle Scholar
  48. Krauhs, J. M., 1979, Structure of rat baroreceptors and their relationship to connective tissue, J. Neurocytol., 8:401–414PubMedCrossRefGoogle Scholar
  49. Krauhs, J. M., 1984, Morphology of presumptive slowly adapting receptors in dog trachea, Anat. Rec., 210:73–85PubMedCrossRefGoogle Scholar
  50. Kuo, D. C., and deGroat, W. C., 1985, Primary afferent projections of the major splanchnic nerve to the spinal cord and gracile nucleus of the cat, J. Comp. Neurol., 231:421–434PubMedCrossRefGoogle Scholar
  51. Leek, B. F., 1969, Reticulo-ruminal mechanoreceptors in sheep, J. Physiol. (Lond.), 202:585–609Google Scholar
  52. Leek, B. F., 1972, Abdominal visceral receptors, in: “Handbook of Sensory Physiology, Vol. 3,” E. Neu, ed., Springer, Berlin: 113–160Google Scholar
  53. Maggi, C. A., and Meli, A., 1988, The sensory-efferent function of capsaicin-sensitive sensory neurons, Gen. Pharmac., 19:1–43Google Scholar
  54. Marfurt, C. F., and Turner, D. F., 1983, Sensory nerve endings in the rat oro-facial region labeled by the anterograde and transganglionic transport of horseradish peroxidase: a new method for tracing peripheral nerve fibers, Brain Res., 261:1–12PubMedCrossRefGoogle Scholar
  55. McDonald, D. M., and Mitchell, R. A., 1975, The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid body: a quantitative ultrastructural analysis, J. Neurocytol., 4:177–230CrossRefGoogle Scholar
  56. Mei, N., 1970, Mécanorécepteurs vagaux digestifs chez le chat, Exp. Brain Res., 11:502–514PubMedGoogle Scholar
  57. Mei, N., 1983, Sensory structures in the viscera, in: “Progress in Sensory Physiology, Vol. 4,” D. Ottoson, ed., Springer, Berlin: 1–42Google Scholar
  58. Mei, N., 1985, Intestinal chemosensitivity, Physiol. Rev., 65:211–237PubMedGoogle Scholar
  59. Mei, N., Aubert, M., Crousillat, J., and Ranieri, F., 1973, Sensory innervation of the lower oesophagus of the cat. Comparison with other parts of the digestive system, Proc. IVth Internat. Symp. Gastrointest. Mot., Banff, CanadaGoogle Scholar
  60. Miolan, J. P., and Niel, J. P., 1988, Involvement of cholinergic neurones in the permanent depolarization of the muscular cells of the lower oesophageal sphincter in the cat in vitro, J. Physiol. (Lond.), 406:138PGoogle Scholar
  61. Mori, K., 1987, Specific carbohydrate expression by small-diameter subclasses of rabbit trigeminal, glossopharyngeal, and vagal afferent fibers studied with the lectin Ulex europaeusagglutinin I, Neurosci. Res., 4:291–303PubMedCrossRefGoogle Scholar
  62. Munger, B. L., and Ide, C., 1987, The enigma of sensitivity in Pacinian corpuscules: a critical review and hypothesis of mechano-electric transduction, Neurosci. Res., 5:1–15PubMedCrossRefGoogle Scholar
  63. Neuhuber, W. L., 1987, Sensory vagal innervation of the rat esophagus and cardia: a light and electron microscopic anterograde tracing study, J. Autonom. Nerv. Syst., 20:243–255CrossRefGoogle Scholar
  64. Nonidez, J. F., 1946, Afferent nerve endings in the ganglia of the intramural plexus of the dog’s oesophagus, J. Comp. Neurol., 85:177–189PubMedCrossRefGoogle Scholar
  65. Robertson, B., and Aldskogius, H., 1982, The use of anterogradery transported wheat germ agglutinin-horseradish peroxidase conjugate to visualize cutaneous sensory nerve endings, Brain Res., 240:327–330PubMedCrossRefGoogle Scholar
  66. Robles-Chillida, E. M., Rodrigo, J., Mayo, I., Arnedo, A., and Gomez, A., 1981, Ultrastructure of free-ending nerve fibers in oesophageal epithelium, J. Anat., 133:227–233PubMedGoogle Scholar
  67. Rodrigo, J., deFelipe, J., Robles-Chillida, E. M., Pérez Anton, J. A., Mayo, I., and Gomez, A., Sensory vagal nature and anatomical access paths to esophagus laminar nerve endings in myenteric ganglia. Determination by surgical degeneration methods, Acta anat., 112:47–57Google Scholar
  68. Rodrigo, J., Hernandez, C. J., Vidal, M. A., and Pedrosa, J. A., 1975, Vegetative innervation of the esophagus. II. Intraganglionar laminar endings, Acta anat., 92:79–100PubMedCrossRefGoogle Scholar
  69. Roman, C., and Gonella, J., 1987, Extrinsic control of digestive tract motility, in: “Physiology of the Gastrointestinal Tract, 2nd Ed.,” L. R. Johnson, ed., Raven Press, New York: 507–553Google Scholar
  70. Sato, M., and Koyano, H., 1987, Autoradiographic study on the distribution of vagal afferent nerve fibers in the gastroduodenal wall of the rabbit, Brain Res., 400:101–109PubMedCrossRefGoogle Scholar
  71. Scarfone, E., Demêmes, D., Jahn, R., De Camilli, P., and Sans, A., 1988, Secretory function of the vestibular nerve calyx suggested by presence of vesicles, synapsin I, and synaptophysin, J. Neurosci., 8:4640–4645PubMedGoogle Scholar
  72. Schnyder, H., and Künzle, H., 1983, Differential labeling in neuronal tracing with wheat germ agglutinin, Neurosci. Lett., 35:115–120PubMedCrossRefGoogle Scholar
  73. Schoultz, T. W., and Swett, J. E., 1974, Ultrastructural organization of the sensory fibers innervating the Golgi tendon organ, Anat. Rec., 179:147–162PubMedCrossRefGoogle Scholar
  74. Stach, W., 1976, Afferente Nervenendigungen im Dünndarm und Magen. Licht- und elektronenmikroskopische Untersuchungen, Z. mikrosk.-anat. Forsch., 90:790–800PubMedGoogle Scholar
  75. Stöhr jr., P., 1957, Mikroskopische Anatomie des vegetativen Nervensystems, in: “Handbuch der mikroskopischen Anatomie des Menschen, Vol. IV/5,” W. Bargmann, ed., Springer, BerlinGoogle Scholar
  76. Wood, J. D., 1987, Physiology of the enteric nervous system, in: “Physiology of the Gastrointestinal Tract, 2nd Ed.,” L. R. Johnson, ed., Raven Press, New York: 67–109Google Scholar

Copyright information

© Plenum Press, New York 1990

Authors and Affiliations

  • Winfried L. Neuhuber
    • 1
  • Nadine Clerc
    • 2
  1. 1.Anatomisches InstitutUniversität Zürich-IrchelZürichSwitzerland
  2. 2.Laboratoire de NeurobiologieC.N.R.S.MarseilleFrance

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