Vagal and spinal afferent innervation of the rat esophagus: A combined retrograde tracing and immunocytochemical study with special emphasis on calcium-binding proteins

Journal of Comparative Neurology

Volumn 398, Issue 2, 1998, Pages 289-307

  Dütsch, Matthias ^a   Eichhorn, Ulrike ^a   Wörl, Jürgen ^a   Wank, Michael ^a   Berthoud, Hans Rudolf ^b   Neuhuber, Winfried L ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Calbindin; Calretinin; Dorsal root ganglion; Fluoro Gold; Nodose ganglion

Indexed keywords

CALBINDIN; CALCITONIN GENE RELATED PEPTIDE; CALCIUM BINDING PROTEIN; CALRETININ; FLUOROGOLD; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ESOPHAGUS; INTESTINE INNERVATION; NODOSE GANGLION; NONHUMAN; PARASYMPATHETIC INNERVATION; PRIORITY JOURNAL; RAT; SENSORY NERVE; SPINAL CORD NERVE CELL; SPINAL GANGLION; VAGUS NERVE;

EID: 2642615359     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980824)398:2<289::AID-CNE9>3.3.CO;2-T     Document Type: Article

References (73)

1. Aimi, Y., M. Fujimura, S.R. Vincent, and H. Kimura (1991) Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat. J. Comp. Neurol. 306:382-392.
2. Aldskogius, H., L.-G. Elfvin, and C. Andersson-Forsman (1986) Primary sensory afferents in the inferior mesenteric ganglion and related nerves of the guinea pig. J. Auton. Nerv. Syst. 15:179-190.
3. Alm, P., B. Uvelius, J. Ekström, B. Holmqvist, B. Larsson, and K.-E. Andersson (1995) Nitric oxide synthase-containing neurons in rat parasympathetic, sympathetic and sensory ganglia: A comparative study. Histochem. J. 27:819-831.
4. Altschuler, S.M., X. Bao, D. Bieger, D.A. Hopkins, and R.R. Miselis (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. 283:248-268.
5. Andressen, C., I. Blümcke, and M.R. Celio (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res. 271:181-208.
6. Andrew, B.L. (1957) Activity in afferent nerve fibers from the cervical oesophagus. J. Physiol. (Lond.) 135:54P-55P.
7. Arai, R., L. Winsky, M. Arai, and D.M. Jacobowitz (1991) Immunohistochemical localization of calretinin in the rat hindbrain. J. Comp. Neurol. 310:21-44.
8. Baimbridge, K.G., M.R. Celio, and J.H. Rogers (1992) Calcium-binding proteins in the nervous system. Trends Neurosci. 15:303-308.
9. Berthoud, H.-R. (1995) Anatomical demonstration of vagal input to nicotinamide acetamide dinucleotide phosphate diaphorase-positive (nitrergic) neurons in rat fundic stomach. J. Comp. Neurol. 385:428-439.
10. Berthoud, H.-R. and W.L. Neuhuber (1994) Distribution and morphology of vagal afferents and efferents supplying the digestive system. In Y. Taché, D.L. Wingate, and T. Burks (eds): Innervation of the Gut; Pathophysiological Implications. Boca Raton, FL: CRC Press, Chapter 4, pp. 43-65.
11. Berthoud, H.-R. and L.M. Patterson (1996) Innervation of rat abdominal paraganglia by calretinin-like immunoreactive nerve fibers. Neurosci. Lett. 210:115-118.
12. Berthoud, H.-R. and T.L. Powley (1992) Vagal afferent innervation of the rat fundic stomach: Morphological characterization of the gastric tension receptor. J. Comp. Neurol. 319:261-276.
13. Berthoud, H.-R., M. Kressel, and W.L. Neuhuber (1995) Vagal afferent innervation of rat abdominal paraganglia as revealed by anterograde Dil-tracing and confocal microscopy. Acta Anat. (Basel) 152:127-132.
14. Berthoud, H.-R., L.M. Patterson, F. Neumann, and W.L. Neuhuber (1997a) Distribution and structure of vagal afferent intraganglionic laminar endings (IGLEs) in the rat gastrointestinal tract. Anat. Embryol. (Berl.) 195:183-191.
15. Berthoud, H.-R., L.M. Patterson, A.E. Willing, K. Müller, and W.L. Neuhuber (1997b) Capsaicin-resistant vagal afferent fibers in the rat gastrointestinal tract: Anatomical identification and functional integrity. Brain Res. 746:195-206.
16. Celio, M.R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
17. Celio, M.R., W. Baier, L. Schärer, H.J. Gregersen, P.A. de Viragh, and A.W. Norman (1990) Monoclonal antibodies directed against the calcium binding protein Calbindin D-28k. Cell Calcium 11:599-602.
18. Christensen, J., G.A. Rick, and D.J. Soll (1987) Intramural nerves and interstitial cells revealed by the Champy-Maillet stain in the opossum esophagus. J. Auton. Nerv. Syst. 19:137-151.
19. Clerc, N. and M. Condamin (1987) Selective labeling of vagal sensory nerve fibers in the lower esophageal sphincter with anterogradely transported WGA-HRP. Brain Res. 424:216-224.
20. Clerc, N. and C. Mazzia (1994) Morphological relationships of choleragenoid horseradish peroxidase-labeled spinal primary afferents with myenteric ganglia and mucosa associated lymphoid tissue in the cat esophagogastric junction. J. Comp. Neurol. 347:171-186.
21. deGroat, W.C. (1986) Spinal cord projections and neuropeptides in visceral afferent neurons. Prog. Brain Res. 67:165-187.
22. Dogiel, A.S. (1899) Ueber den Bau der Ganglien in den Geflechten des Darmes und der Gallenblase des Menschen und der Säugethiere. Arch. Anat. Entwickl.-Gesch. 1899: 130-158.
23. Due, C., I. Barakat-Walter, and B. Droz (1994) Innervation of putative rapidly adapting mechanosensors by Calbindin-and calretinin-immunoreactive primary sensory neurons in the rat. Eur. J. Neurosci. 6:264-271.
24. Dütsch, M., S. Heist, J. Wörl, and W.L. Neuhuber (1994) Distribution of calretinin in the upper digestive tract of rats and humans: A selective marker for vagal afferents? Acta Anat. (Basel) 149:150-151.
25. Dütsch, M., J. Wörl, U. Eichhorn, M. Kressel, and W.L. Neuhuber (1997) Calretinin as a marker for vagal afferent nerve fibers in the rat esophagus. J. Auton. Nerv. Syst. 65:154.
26. Green, T. and G.J. Dockray (1987) Calcitonin gene-related peptide and substance P in afferents to the upper gastrointestinal tract in the rat. Neurosci. Lett. 76:151-156.
27. Helke, C.J. and K.M. Hill (1988) Immunohistochemical study of neuropeptides in vagal and glossopharyngeal afferent neurons in the rat. Neuroscience 26:539-551.
28. Helke, C.J. and A.J. Niederer (1990) Studies on the coexistence of substance P with other putative transmitters in the nodose and petrosal ganglia. Synapse 5:144-151.
29. Holst, M.-C., J.B. Kelly, and T.L. Powley (1997) Vagal preganglionic projections to the enteric nervous system characterized with Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 381:81-100.
30. Holzer, P. (1988) Local effector functions of capsaicin-sensitive sensory nerve endings: Involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24: 739-768.
31. Honda, C.N. (1995) Differential distribution of calbindin-D28k and parvalbumin in somatic and visceral sensory neurons. Neuroscience 68:883-892.
32. Ichikawa, H. and C.J. Helke (1995) Parvalbumin and calbindin D-28k in vagal and glossopharyngeal sensory neurons of the rat. Brain Res. 675:337-341.
33. Ichikawa, H. and C.J. Helke (1996) Coexistence of calbindin D-28k and NADPH-diaphorase in vagal and glossopharyngeal sensory neurons of the rat. Brain Res. 735:325-329.
34. Ichikawa, H., D.M. Jacobowitz, L. Winsky, and C.J. Helke (1991) Calretinin-immunoreactivity in vagal and glossopharyngeal sensory neurons of the rat: Distribution and coexistence with putative transmitter agents. Brain Res. 557:316-322.
35. Jänig, W. and J.F.B. Morrison (1986) Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception. Prog. Brain Res. 67:87-114.
36. Kashiba, H., E. Senba, Y. Ueda, and M. Tohyama (1990) Calbindin D28k-containing splanchnic and cutaneous dorsal root ganglion neurons in the rat. Brain Res. 528:311-316.
37. Kazimierczak, J., E.W. Sommer, E. Philippe, and B. Droz (1986) Carbonic anhydrase activity in primary sensory neurons. I. Requirements for the cytochemical localization in the dorsal root ganglion of chicken and mouse by light and electron microscopy. Cell Tissue Res. 245:487-495.
38. Kressel, M. (1998) Tyramide amplification allows anterograde tracing by horseradish peroxidase-conjugated lectins in conjunction with simultaneous immunohistochemistry. J. Histochem. Cytochem. 46: 527-534.
39. Kressel, M., H.-R. Berthoud, and W.L. Neuhuber (1994) Vagal innervation of the rat pylorus: an anterograde tracing study using carbocyanine dyes and laser scanning confocal microscopy. Cell Tissue Res. 275:109-123.
40. Kummer, W., A. Fischer, R. Kurkowski, and C. Heym (1992) The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry. Neuroscience 49:715-737.
41. Kummer, W., S. Bachmann, W.L. Neuhuber, J. Hänze, and R.E. Lang (1993) Tyrosine-hydroxylase-containing vagal afferent neurons in the rat nodose ganglion are independent from neuropeptide-Y-containing populations and project to esophagus and stomach. Cell Tissue Res. 271:135-144.
42. Kuramoto, H. and R. Kuwano (1994) Immunohistochemical demonstration of calbindin-containing nerve endings in the rat esophagus. Cell Tissue Res. 278:57-64.
43. Kuramoto, H. and R. Kuwano (1995) Location of sensory nerve cells that provide calbindin-containing laminar nerve endings in myenteric ganglia of the rat esophagus. J. Auton. Nerv. Syst. 54:126-136.
44. Lindh, B., C.-J. Dalsgaard, L.-G. Elfvin, T. Hökfelt, and A.C. Cuello (1983) Evidence of substance P immunoreactive neurons in dorsal root ganglia and vagal ganglia projecting to the guinea pig pylorus. Brain Res. 269:365-369.
45. Lindh, B., H. Aldskogius, and T. Hökfelt (1989) Simultaneous immunohistochemical demonstration of intra-axonally transported markers and neuropeptides in the peripheral nervous system of the guinea pig. Histochemistry 92:367-376.
46. Lü, Y., Y.-Q. Ding, B.-Z. Qin, and J.-S. Li (1994) The distribution and origin of axon terminals with NADPH diaphorase activity in the nucleus of the solitary tract of the rat. Neurosci. Lett. 171:70-72.
47. Mazzia, C. and N. Clerc (1997) Ultrastructural relationships of spinal primary afferent fibers with neuronal and non-neuronal cells in the myenteric plexus of the cat oesophago-gastric junction. Neuroscience 80:925-937.
48. Miller, R.J. (1995) Regulation of calcium homeostasis in neurons: The role of calcium-binding proteins. Biochem. Soc. Trans. 23:629-632.
49. Neuhuber, W.L. (1987) Sensory vagal innervation of the rat esophagus and cardia: A light and electron microscopic anterograde tracing study. J. Auton. Nerv. Syst. 20:243-255.
50. Neuhuber, W.L., and N. Clerc (1990) Afferent innervation of the esophagus in cat and rat. In W. Zenker and W.L. Neuhuber (eds): The Primary Afferent Neuron. A Survey of Recent Morpho-Functional Aspects. New York: Plenum Press, pp. 93-107.
51. Neuhuber, W.L., M. Kressel, M. Dütsch, J. Wörl, and H.-R. Berthoud (1995) Relationships of IGLEs to enteric glia and neurons in the rat esophagus: Further indications of a mechanosensor-local effector role. Soc. Neurosci. Abstr. 21:1633.
52. Neuhuber, W.L., M. Kressel, A. Stark, and H.-R. Berthoud (1998) Vagal efferent and afferent innervation of the rat esophagus as demonstrated by anterograde Dil and DiA tracing: focus on myenteric ganglia. J. Auton. Nerv. Syst. (in press).
53. Nonidez, J.F. (1946) Afferent nerve endings in the ganglia of the intermuscular plexus of the dog's oesophagus. J. Comp. Neurol. 85:177-189.
54. Phillips, R.J., E.A. Baronowski, and T.L. Powley (1997) Afferent innervation of the gastrointestinal tract smooth muscle by the hepatic branch of the vagus. J. Comp. Neurol. 384:248-270.
55. Powley, T.L. and H.-R. Berthoud (1991) A fluorescent labeling strategy for staining the enteric nervous system. J. Neurosci. Methods 36:9-15.
56. Rodrigo, J., C.J. Hernandez, M.A. Vidal, and J.A. Pedrosa (1975) Vegetative innervation of the esophagus. II. Intraganglionic laminar endings. Acta Anat. (Basel) 92:79-100.
57. Rodrigo, J., J.M. Polak, L. Fernandez, M.A. Ghatei, P. Mulderry, and S.R. Bloom (1985) Calcitonin gene-related peptide immunoreactive sensory and motor nerves of the rat, cat and monkey esophagus. Gastroenterology 88:444-451.
58. Rodrigo, J., J. deFelipe, E.M. Robles-Chillida, J.A. PérezAnton, I. Mayo, and A. Gomez (1982) Sensory vagal nature and anatomical access paths to esophagus laminar endings in myenteric ganglia. Determination by surgical degeneration methods. Acta Anat. (Basel) 112:47-57.
59. Rogers, J.H. (1987) Calretinin: A gene for a novel calcium-binding protein expressed principally in neurons. J. Cell Biol. 105:1343-1353.
60. Ruggiero, D.A., E.P. Muti, K. Otake, and M. Anwar (1996) Central and primary visceral afferents to nucleus tractus solitarii may generate nitric oxide as a membrane-permeant neuronal messenger. J. Comp. Neurol. 364:51-67.
61. Scherer-Singler, U., S.R. Vincent, H. Kimura, and E.G. McGeer (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Methods 9:229-234.
62. Schwaller, B., P. Buchwald, I. Blümcke, M.R. Celio, and W. Hunziker (1993) Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium 74:639-648.
63. Sengupta, J.N., D. Kauvar, and R.K. Goyal (1989) Characteristics of vagal esophageal tension-sensitive afferent fibers in the opossum. J. Neuro-physiol. 61:1001-1010.
64. Shapiro, R.E. and R.R. Miselis (1985) The central organization of the vagus nerve innervating the stomach of the rat. J. Comp. Neurol. 238:473-488.
65. Springall, D.R., A. Cadieux, H. Oliveira, H. Su, D. Royston, and J.M. Polak (1987) Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J. Auton. Nerv. Syst. 20:155-166.
66. Stach, W. (1989) A revised morphological classification of neurons in the enteric nervous system. In M.V. Singer and H. Goebell (eds): Nerves and the Gastrointestinal Tract. Dordrecht: MTP Press, pp. 29-45.
67. Sternini, C. (1988) Structural and chemical organization of the myenteric plexus. Annu. Rev. Physiol. 50:81-93.
68. Sternini, C. (1992) Vagal afferent innervation of the enteric nervous system. In S. Ritter, R.C. Ritter, and C.D. Barnes (eds): Neuroanatomy and Physiology of Abdominal Vagal Afferents. Boca Raton: CRC Press, pp. 136-156.
69. Stökr, Jr., P. (1957) Mikroskopische Anatomie des vegetoliver Nerven Systems. In W. Bargmann (ed): Handbuch der Mikroskopischein Anatouire des Menschen. Vol IV 15. Berlin: Springer, pp. 323-334.
70. Uddman, R., T. Grunditz, A. Luts, H. Desai, G. Fernström, and F. Sundler (1995) Distribution and origin of the peripheral innervation of rat cervical esophagus. Dysphagia 10:203-212.
71. Vincent, S.R. and H. Kimura (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755-784.
72. Yamamoto, Y., I. Hosono, Y. Atoji, and Y. Suzuki (1997) Morphological study of the vagal afferent nerve endings in the laryngeal mucosa of the dog. Ann. Anat. 179:65-73.
73. Zhuo, H., H. Ichikawa, and C.J. Helke (1997) Neurochemistry of the nodose ganglion. Prog. Neurobiol. 52:79-107.