Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1982 Feb;79(4):1303–1307. doi: 10.1073/pnas.79.4.1303

Organizational principles in the peripheral sympathetic nervous system: Subdivision by coexisting peptides (somatostatin-, avian pancreatic polypeptide-, and vasoactive intestinal polypeptide-like immunoreactive materials

J M Lundberg *, T Hökfelt , A Änggård , L Terenius §, R Elde , K Markey ǁ, M Goldstein ǁ, J Kimmel **
PMCID: PMC345951  PMID: 6122210

Abstract

Sympathetic ganglia and some peripheral tissues of adult guinea pig and cat were analyzed by the indirect immunofluorescence technique with antisera to catecholamine-synthesizing enzymes and some peptides. In the guinea pig, noradrenergic neurons could be subdivided into three populations containing respectively (i) somatostatin-like immunoreactive material, (ii) avian pancreatic polypeptide (APP)-like immunoreactive material, and (iii) apparently only noradrenaline (NA; norepinephrine). A fourth population of sympathetic neurons was nonadrenergic and contained vasoactive intestinal polypeptide (VIP)-immunoreactive material. In the cat many noradrenergic neurons with APP and some without this peptide were seen, but no somatostatin-immunoreactive neurons were observed. Also a population of non-adrenergic, presumably cholinergic, neurons containing a VIP-like peptide was observed. These neuron populations seemed to innervate different tissues with some target specificity. For example, in the nasal mucosa of the cat, nerves containing NA/APP-like immunoreactive material (called NA/APP nerves) were found around small arteries and arterioles, whereas venules and sinusoids were surrounded by nerves containing only NA (called NA nerves). Also in the submandibular salivary gland of the cat, the NA/APP nerves surrounded arteries and arterioles, whereas NA nerves were seen in relation to acini and ducts. The sympathetic (cholinergic) VIP-containing neurons innervated blood vessels and exocrine tissue in the cat sweat glands. In the coeliac-superior mesenteric ganglion complex of the guinea pig and cat, a dense network of VIP-immunoreactive fibers was seen preferentially around noradrenergic ganglionic cell bodies lacking APP-immunoreactive material. Thus, adult peripheral sympathetic neurons can be subdivided into several categories on the basis of specific peptides. These subdivisions may innervate specific targets and may receive peptide-specific neuronal inputs.

Keywords: neuronal organization, peptide multiplicity

Full text

PDF
1303

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anggård A., Edwall L. The effects of sympathetic nerve stimulation on the tracer disappearance rate and local blood content in the nasal mucosa of the cat. Acta Otolaryngol. 1974 Jan-Feb;77(1):131–139. doi: 10.3109/00016487409124608. [DOI] [PubMed] [Google Scholar]
  2. Arimura A., Lundqvist G., Rothman J., Chang R., Fernandez-Durango R., Elde R., Coy D. H., Schally A. V., Meyers C. Radioimmunoassay of somatostatin. Metabolism. 1978 Sep;27(9 Suppl 1):1139–1144. doi: 10.1016/0026-0495(78)90032-x. [DOI] [PubMed] [Google Scholar]
  3. COONS A. H. Fluorescent antibody methods. Gen Cytochem Methods. 1958;1:399–422. [PubMed] [Google Scholar]
  4. Chan-Palay V., Jonsson G., Palay S. L. Serotonin and substance P coexist i, neurons of the rat's central nervous system. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1582–1586. doi: 10.1073/pnas.75.3.1582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dahlström A. Effects of vinblastine and colchicine on monoamine containing neurons of the rat, with special regard to the axoplasmic transport of amine granules. Acta Neuropathol. 1971;5(Suppl):226–237. doi: 10.1007/978-3-642-47449-1_28. [DOI] [PubMed] [Google Scholar]
  6. Dale H. H., Feldberg W. The chemical transmission of secretory impulses to the sweat glands of the cat. J Physiol. 1934 Aug 24;82(1):121–128. doi: 10.1113/jphysiol.1934.sp003166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hartman B. K., Zide D., Udenfriend S. The use of dopamine -hydroxylase as a marker for the central noradrenergic nervous system in rat brain. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2722–2726. doi: 10.1073/pnas.69.9.2722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hökfelt T., Elfvin L. G., Elde R., Schultzberg M., Goldstein M., Luft R. Occurrence of somatostatin-like immunoreactivity in some peripheral sympathetic noradrenergic neurons. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3587–3591. doi: 10.1073/pnas.74.8.3587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hökfelt T., Johansson O., Ljungdahl A., Lundberg J. M., Schultzberg M. Peptidergic neurones. Nature. 1980 Apr 10;284(5756):515–521. doi: 10.1038/284515a0. [DOI] [PubMed] [Google Scholar]
  10. Hökfelt T., Ljungdahl A., Steinbusch H., Verhofstad A., Nilsson G., Brodin E., Pernow B., Goldstein M. Immunohistochemical evidence of substance P-like immunoreactivity in some 5-hydroxytryptamine-containing neurons in the rat central nervous system. Neuroscience. 1978;3(6):517–538. doi: 10.1016/0306-4522(78)90017-9. [DOI] [PubMed] [Google Scholar]
  11. Hökfelt T., Lundberg J. M., Schultzberg M., Johansson O., Ljungdahl A., Rehfeld J. Coexistence of peptides and putative transmitters in neurons. Adv Biochem Psychopharmacol. 1980;22:1–23. [PubMed] [Google Scholar]
  12. Langley J. N. On the Course and Connections of the Secretory Fibres supplying the Sweat Glands of the Feet of the Cat. J Physiol. 1891 Sep;12(4):347–390.17. doi: 10.1113/jphysiol.1891.sp000388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lundberg J. M., Anggård A., Fahrenkrug J., Hökfelt T., Mutt V. Vasoactive intestinal polypeptide in cholinergic neurons of exocrine glands: functional significance of coexisting transmitters for vasodilation and secretion. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1651–1655. doi: 10.1073/pnas.77.3.1651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lundberg J. M. Evidence for coexistence of vasoactive intestinal polypeptide (VIP) and acetylcholine in neurons of cat exocrine glands. Morphological, biochemical and functional studies. Acta Physiol Scand Suppl. 1981;496:1–57. [PubMed] [Google Scholar]
  15. Lundberg J. M., Hökfelt T., Anggård A., Kimmel J., Goldstein M., Markey K. Coexistence of an avian pancreatic polypeptide (APP) immunoreactive substance and catecholamine in some peripheral and central neurons. Acta Physiol Scand. 1980 Sep;110(1):107–109. doi: 10.1111/j.1748-1716.1980.tb06638.x. [DOI] [PubMed] [Google Scholar]
  16. Lundberg J. M., Hökfelt T., Anggård A., Uvnäs-Wallensten K., Brimijoin S., Brodin E., Fahrenkrug J. Peripheral peptide neurons: distribution, axonal transport, and some aspects on possible function. Adv Biochem Psychopharmacol. 1980;22:25–36. [PubMed] [Google Scholar]
  17. Lundberg J. M., Hökfelt T., Schultzberg M., Uvnäs-Wallensten K., Köhler C., Said S. I. Occurrence of vasoactive intestinal polypeptide (VIP)-like immunoreactivity in certain cholinergic neurons of the cat: evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience. 1979;4(11):1539–1559. doi: 10.1016/0306-4522(79)90018-6. [DOI] [PubMed] [Google Scholar]
  18. MELLANDER S. Comparative studies on the adrenergic neuro-hormonal control of resistance and capacitance blood vessels in the cat. Acta Physiol Scand Suppl. 1960;50(176):1–86. [PubMed] [Google Scholar]
  19. Markey K. A., Kondo H., Shenkman L., Goldstein M. Purification and characterization of tyrosine hydroxylase from a clonal pheochromocytoma cell line. Mol Pharmacol. 1980 Jan;17(1):79–85. [PubMed] [Google Scholar]
  20. Szurszewski J. H. Physiology of mammalian prevertebral ganglia. Annu Rev Physiol. 1981;43:53–68. doi: 10.1146/annurev.ph.43.030181.000413. [DOI] [PubMed] [Google Scholar]
  21. Tramu G., Pillez A., Leonardelli J. An efficient method of antibody elution for the successive or simultaneous localization of two antigens by immunocytochemistry. J Histochem Cytochem. 1978 Apr;26(4):322–324. doi: 10.1177/26.4.207771. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES