Skip to main content
SpringerLink
Log in

The sympathetic superior cervical ganglia as peripheral neuroendocrine centers

  • Review Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Summary

The superior cervical ganglia (SCG) provide sympathetic innervation to the pineal gland, cephalic blood vessels, the choroid plexus, the eye, carotid body and the salivary and thyroid glands. Removal of the ganglia brings about several neuroendocrine changes in mammals, including the disruption of water balance in pituitary stalk-sectioned rats, and the alteration of normal photoperiodic control of reproduction in hamsters, ferrets, voles, rams and goats. These effects are commonly attributed to pineal denervation. However pinealectomy does not always mimic ganglionectomy in its neuroendocrine sequelae. This paper discusses several examples illustrating the lack of homology of ganglia and pineal removal, including the prolactin release brought about by gonadal steroids in spayed rats, the changes in drinking behaviour caused by ganglionectomy and the control of goitrogenic response to methylmercaptoimidazole in rats. All these examples indicate that SCG removal, at least as far as for neuroendocrinologists and pineal experimenters are concerned, should not be considered simply as “pineal denervation”. A functionally relevant link between SCG and the hypothalamus may occur in rats inasmuch as ganglionectomy depresses norepinephrine uptake and increases the number and responses afα-adrenoceptors in medial basal hypothalamus. Lastly the SCG are active points of concurrency for hormone signals, as revealed by the metabolic changes induced by steroid and anterior pituitary hormones in these structures even in the absence of intact preganglionic connections, as well as by the existence of putative receptors for some of the hormones, namely, estradiol, testosterone and corticosteroids. The SCG appear to constitute a peripheral neuroendocrine center.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Alper, R. H., Demarest, K. T., Moore, K. E.: Effect of surgical sympathectomy on catecholamine concentration in the posterior pituitary of the rat. Experientia36, 134–135 (1980).

    PubMed  Google Scholar 

  2. Baum, M. J.: Light synchronization of rat feeding rhythms following sympathectomy or pinealectomy. Physiol. Behav.5, 325–329 (1970).

    PubMed  Google Scholar 

  3. Benoit, J., Assenmacher, I.: Le controle hypothalamique de l'activité préhypophysaire gonadotrope. J. Physiol. (Paris)47, 427–567 (1955).

    Google Scholar 

  4. Bergland, R. M., Page, R. B.: Pituitary-brain vascular relations: a new paradigm. Science204, 18–24 (1979).

    PubMed  Google Scholar 

  5. Björklund, A.: Monoamine-containing fibres in the pituitary neurointermediate lobe of the pig and the rat. Z. Zellforsch.89, 573–589 (1968).

    PubMed  Google Scholar 

  6. Björklund, A., Moore, R. Y., Nobin, A., Stenevi, U.: The organization of tubero-hypophyseal and reticulo-infundibular catecholamine neuron systems in the rat brain. Brain Res.51, 171–179 (1973).

    PubMed  Google Scholar 

  7. Björklund, A., Owman, Ch., West, K. A.: Peripheral sympathetic innervation and serotonin cells in the habenular region of the rat brain. Z. Zellforsch.127, 570–579 (1972).

    PubMed  Google Scholar 

  8. Black, I. B.: Regulation of the growth and development of sympathetic neuronsin vivo. In: Progress in Clinical and Biological Research (Hall, Z., Kelly, R., Fox, C. F., eds.), Vol. 15: Cellular Neurobiology, pp. 61–71. New York: Alan R. Liss. 1977.

    Google Scholar 

  9. Brooks, C. McC., Koizumi, K., Sato, A. (eds.): Integrative Function of the Autonomic Nervous System. Tokyo: University of Tokyo Press. 1979.

    Google Scholar 

  10. Buttle, H. L.: The effect of anterior cervical ganglionectomy on the seasonal variation in prolactin concentration in goats. Neuroendocrinology23, 121–128 (1977).

    PubMed  Google Scholar 

  11. Cardinali, D. P.: Changes in hypothalamic neurotransmitter uptake following pinealectomy, superior cervical ganglionectomy or melatonin administration to rats. Neuroendocrinology19, 91–95 (1975).

    PubMed  Google Scholar 

  12. Cardinali, D. P.: Models in neuroendocrinology: neurohumoral pathways to the pineal gland. Trends Neurosci.2, 250–252 (1979).

    Google Scholar 

  13. Cardinali, D. P.: Melatonin. A mammalian pineal hormone. Endocrine Rev. (1981, in press).

  14. Cardinali, D. P., Faigón, M. R., Scacchi, P., Moguilevsky, J.: Failure of melatonin to increase plasma prolactin levels in ovariectomized rats subjected to superior cervical ganglionectomy or pinealectomy. J. Endocrinol.82, 315–319 (1979).

    PubMed  Google Scholar 

  15. Cardinali, D. P., Freire, F., Nagle, C. A., Rosner, J. M.: Effects of environmental lighting, superior cervical ganglionectomy and adrenergic drugs on microtubule protein levels of the rat hypothalamus. Neuroendocrinology19, 44–53 (1975).

    PubMed  Google Scholar 

  16. Cardinali, D. P., Vacas, M. I.: Norepinephrine turnover in pineal gland and superior cervical ganglia. Changes after gonadotrophin administration to castrated rats. J. Neural Transm.45, 273–284 (1979).

    PubMed  Google Scholar 

  17. Cardinali, D.P., Vacas, M.I., Fortis, A.L., Stéfano, F. J.: Superior cervical ganglionectomy depresses norepinephrine uptake, increases the density ofα-adrenoceptor sites, and induces supersensitivity to adrenergic drugs in rat medial basal hypothalamus. Neuroendocrinology (1981, in press).

  18. Cardinali, D. P., Vacas, M. I., Valenti, C. E., Solveyra, C. G.: Pineal gland and sympathetic cervical ganglia as sites for steroid regulation of photosensitive neuroendocrine pathways. J. Steroid Biochem.11, 951–955 (1979).

    PubMed  Google Scholar 

  19. Charlton, H. M., Grocock, A. C., Ostberg, A.: The effect of pinealectomy and superior cervical ganglionectomy on the testis of the vole,Microtus agrestis. J. Reprod. Fert.48, 377–379 (1976).

    Google Scholar 

  20. Ciaranello, R. D., Jacobowitz, D., Axelrod, J.: Effect of dexamethasone on phenylethanolamine-N-methyltransferase in chromaffin tissue of the neonatal rat. J. Neurochem.20, 799–805 (1973).

    PubMed  Google Scholar 

  21. Dibner, M. D., Black, I.: Biochemical and morphological effects of testosterone treatment on developing sympathetic neurons. J. Neurochem.30, 1479–1483 (1978).

    Google Scholar 

  22. Dolivo, M.: Metabolism of mammalian sympathetic ganglia. Fed. Proc.33, 1043–1048 (1974).

    PubMed  Google Scholar 

  23. Duckles, S. P.: Functional activity of the noradrenergic innervation of large cerebral arteries. Br. J. Pharmac.69, 193–199 (1980).

    Google Scholar 

  24. Eränkö, O., Eränkö, L., Hervonen, H.: Cultures of sympathetic ganglia and the effect of glucocorticoids on SIF cells. In: SIF Cells. Structure and Function of Small, Intensely Fluorescent Sympathetic Cells (Eränkö, O., ed.), pp. 196–214. Washington, D.C.: US Government Printing Office. 1976.

    Google Scholar 

  25. Falck, B., Mchedlishvili, G. I., Owman, Ch.: Histochemical demonstration of adrenergic nerves in cortex-pia of rabbit. Acta Pharmacol. (Kbh.)23, 133–142 (1965).

    Google Scholar 

  26. Fendler, K., Vermes, I., Stark, A., Lissák, K.: Effect of cervical sympathectomy on water balance in pituitary stalk-sectioned rats. Acta Physiol. Hung.42, 61–65 (1972).

    Google Scholar 

  27. Friedgood, H. B.: The nervous control of the anterior hypophysis. J. Reprod. Fertil., Suppl.10, 3–14 (1970).

    Google Scholar 

  28. Friedman, A. H., Davis, J. N.: Identification and characterization of adrenergic receptors and catecholamine-stimulated adenylate cyclase in hog pial membranes. Brain Res.183, 89–102 (1980).

    PubMed  Google Scholar 

  29. Gejman, P. V., Cardinali, D. P., Finkielman, S., Nahmod, V. E.: Changes in drinking dehavior caused by superior cervical ganglionectomy and pinealectomy in rats. J. Auton. Nerv. System (1981, in press).

  30. Gianutsos, G., Moore, K. E.: Effects of pre- or postnatal dexamethasone, adrenocorticotrophic hormone and environmental stress on phenylethanolamine-N-methyltransferase activity and catecholamine in sympathetic ganglia of neonatal rats. J. Neurochem.28, 935–940 (1977).

    PubMed  Google Scholar 

  31. Hanbaver, I., Lovenberg, W., Guidotti, A., Costa, E.: Role of cholinergic and glucocorticosteroid receptors in the tyrosine hydroxylase induction elicited by reserpine in superior cervical ganglion. Brain Res.96, 197–200 (1975).

    PubMed  Google Scholar 

  32. Herbert, J.: The pineal gland and light-induced oestrus in ferrets. J. Endocrinol.43, 625–630 (1969).

    PubMed  Google Scholar 

  33. Hubbard, J. (ed.): The Peripheral Nervous System. New York: Plenum. 1974.

    Google Scholar 

  34. Kappers, J. A.: The mammalian pineal gland, a survey. Acta Neurochirurgica34, 109–149 (1976).

    PubMed  Google Scholar 

  35. Knigge, K. M., Scott, D. E., Kobayashi, H. (eds.): Brain-Endocrine Interaction. II. The Ventricular System in Neuroendocrine Mechanisms. Basel: Karger. 1975.

    Google Scholar 

  36. Koslow, S. H., Bjegovic, M., Costa, E.: Catecholamines in sympathetic ganglia of rat: effect of dexamethasone and reserpine. J. Neurochem.24, 277–281 (1975).

    PubMed  Google Scholar 

  37. Lempinen, M.: Extra-adrenal chromaffin tissue of the rat and the effect of cortical hormones on it. Acta Physiol. Scand.62, Suppl. 231 (1964).

  38. Libet, B.: Slow postsynaptic actions in ganglionic functions. In: Integrative Functions of the Autonomic Nervous System (Brooks, C. Mc. C., Koizumi, K., Sato, A., eds.), pp. 197–222. Tokyo: University of Tokyo Press. 1979.

    Google Scholar 

  39. Lincoln, G. A.: Photoperiodic control of seasonal breeding in the ram: participation of the cranial sympathetic nervous system. J. Endocrinol.82, 135–147 (1979).

    PubMed  Google Scholar 

  40. Lindvall, M., Edvinsson, L., Owman, Ch.: Sympathetic nervous control of cerebrospinal fluid production from the choroid plexus. Science201, 176–178 (1978).

    PubMed  Google Scholar 

  41. Marchisio, P. C.: Embryological development of metabolic systems in sympathetic ganglia. Fed. Proc.33, 1039–1042 (1974).

    PubMed  Google Scholar 

  42. Markey, K. A., Sze, P. Y.: Adrenal influence on tyrosine hydroxylase activity in superior cervical ganglion. Brain Res.202, 347–356 (1980).

    PubMed  Google Scholar 

  43. Matthews, M. R.: Synaptic and other relationship of small granulecontaining cells (SIF) in sympathetic ganglia. In: Chromaffin, Enterochromaffin and Related Cells (Coupland, R. E., Fujita, T., eds.), pp. 131–146. Amsterdam: Elsevier. 1976.

    Google Scholar 

  44. McDonald, D. M.: Structure and functions of reciprocal synapses interconnecting glomus cells and sensory nerve terminals in the rat carotid body. In: Chromaffin, Enterochromaffin and Related Cells (Coupland, R. E., Fujita, T., eds.), pp. 375–394. Amsterdam: Elsevier. 1976.

    Google Scholar 

  45. Melander, A., Ericson, L. E., Sundler, F.: Sympathetic regulation of thyroid hormone secretion. Life Sci.14, 237–246 (1974).

    PubMed  Google Scholar 

  46. Moore, R. Y.: The innervation of the mammalian pineal gland. Prog. Reprod. Biol.4, 1–29 (1978).

    Google Scholar 

  47. Nir, I., Reiter, R. J., Wurtman, R. J. (eds.): The Pineal Gland. Wien-New York: Springer. 1978.

    Google Scholar 

  48. Ochs, S., Worth, R. M.: Axoplasmic transport in normal and pathological systems. In: Physiology and Pathobiology of Axons (Waxman, S. G., ed.), pp. 251–264. New York: Raven Press. 1978.

    Google Scholar 

  49. Otten, U., Thoenen, H.: Circadian rhythm of tyrosine hydroxylase induction by short-term cold stress: modulatory action of glucocorticoids in newborn and adult rats. Proc. Nat. Acad. Sci. U.S.A.72, 1415–1419 (1975).

    Google Scholar 

  50. Otten, U., Thoenen, H.: Modulatory role of glucocorticoids on nerve growth factor mediated enzyme induction in organ cultures of sympathetic ganglia. Brain Res.111, 438–441 (1976).

    PubMed  Google Scholar 

  51. Owman, Ch., Edvinsson, L., Falck, B., Nielsen, K. C.: Amine metabolism in brain vessels with particular regard to autonomic innervation and blood-brain barrier. In: Pathology of Cerebral Microcirculation (Navarro, J., ed.), pp. 184–199. Berlin: W. deGruyter. 1974.

    Google Scholar 

  52. Pisarev, M. A., Cardinali, D. P., Juvenal, G. J., Vacas, M. I., Barontini, M., Boado, R. J.: The role of the sympathetic nervous system in the control of the goitrogenic response in the rat. Endocrinology (1981, in press).

  53. Reiter, R. J.: The pineal and its hormones in the control of reproduction. Endocrine Rev.1, 109–131 (1980).

    Google Scholar 

  54. Reiter, R. J., Hester, R. J.: Interrelationships of the pineal gland, the superior cervical ganglia and the photoperiod in the regulation of the endocrine systems of hamsters. Endocrinology79, 1168–1170 (1966).

    PubMed  Google Scholar 

  55. Roel, L. E., Schwartz, S., Weiss, B. F., Munro, H. N., Wurtman, R. J.: In vivo inhibition of rat brain protein synthesis by L-dopa. J. Neurochem.23, 233–239 (1974).

    PubMed  Google Scholar 

  56. Saper, C. B.: Anatomical substrate for the hypothalamic control of the autonomic nervous system. In: Integrative Functions of the Autonomic Nervous System (Brooks, C. Mc. C, Koizumi, K., Sato, A., eds.), pp. 333–341. Tokyo: University of Tokyo Press. 1979.

    Google Scholar 

  57. Sato, T., Sato, S., Suzuki, J.: Correlation with superior cervical sympathetic ganglion and sympathetic nerve innervation of intracranial artery-electron microscopic studies. Brain Res.188, 33–41 (1980).

    PubMed  Google Scholar 

  58. Skok, V. I., Selyanko, A. A.: Acetylcholine and serotonin receptors in mammalian sympathetic ganglion neurons. In: Integrative Functions of the Autonomic Nervous System (Brooks, C. Mc. C., Koizumi, K., Sato, A., eds.), pp. 248–253. Tokyo: University of Tokyo Press. 1979.

    Google Scholar 

  59. Svendgaard, N.-A., Edvinsson, L., Olin, T., Owman, Ch., Salin, Ch.: On the pathophysiology of cerebral vasospasm: transmitter changes in perivascular sympathetic nerves, and increased pial artery sensitivity to norepinephrine and serotonin. In: Neurogenic Control of the Brain Circulation (Owman, Ch., Edvinsson, L., eds.), pp. 143–152. Oxford: Pergamon Press. 1977.

    Google Scholar 

  60. Towle, A. C., Sze, P. Y., Lander, J. M.: Cytosol glucocorticoid receptors in monoaminergic cell groups. Trans. Amer. Soc. Neurochem.10, 119 (1979).

    Google Scholar 

  61. Trendelenburg, U.: Factors influencing the concentration of catecholamines at the receptors. In: Handbook of Experimental Pharmacology (Blaschko, H., Muscholl, E., eds.), pp. 726–771. New York: Springer. 1972.

    Google Scholar 

  62. U'Prichard, D. C., Reisine, T. D., Mason, S. T., Fibiger, H. C., Yamamura, H. I.: Modulation of rat brainα- andβ-adrenergic receptor populations by lesion of the dorsal noradrenergic bundle. Brain Res.187, 143–154 (1980).

    PubMed  Google Scholar 

  63. Vacas, M. I., Cardinali, D. P.: Effects of castration and reproductive hormones on pineal serotonin metabolism in rats. Neuroendocrinology28, 187–195 (1979).

    PubMed  Google Scholar 

  64. Vacas, M. I., Lowenstein, P. R., Cardinali, D. P.: Characterization of a cytosol progesterone receptor in bovine pineal gland. Neuroendocrinology29, 84–89 (1979).

    PubMed  Google Scholar 

  65. Valenti, C., Lombardo, R. J., Libertun, C., Cardinali, D. P.: Changes in total and polymerized tubulin of the medial basal hypothalamus and adenohypophysis of castrated or hormone-injected rats. Experientia36, 1012–1013 (1980).

    PubMed  Google Scholar 

  66. Waymire, J., Bjur, R., Weiner, N.: Assay of tyrosine hydroxylase by coupled decarboxylation of dopa formed from 1-14C-l-tyrosine. Anal. Biochem.43, 588–598 (1971).

    PubMed  Google Scholar 

  67. Williams, T. F., Black, A. C., Chiba, T., Jew, J.: Interneurons/SIF cells in sympathetic ganglia of various mammals. In: Chromaffin, Enterochromaffin and Related Cells (Coupland, R. E., Fujita, T., eds.) pp. 95–116. Amsterdam: Elsevier. 1976.

    Google Scholar 

  68. Zisapel, N., Levi, M., Gozes, I.: Tubulin an integral protein of mammalian synaptic vesicle membrane. J. Neurochem.34, 26–32 (1980).

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. D. P. Cardinali (Established Investigator, CONICET)

    Present address: Centro de Estudios Farmacológicos y de Principios Naturales (CEFAPRIN), Buenos Aires, Argentina

Authors and Affiliations

  1. Centro de Estudios Farmacológicos y de Principios Naturales (CEFAPRIN), Buenos Aires, Argentina

    María I. Vacas & P. V. Gejman (Post-doctoral Research Fellow, CONICET)

Authors
  1. D. P. Cardinali
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María I. Vacas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. V. Gejman
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Studies from author's laboratory were supported by grant no. 6638, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cardinali, D.P., Vacas, M.I. & Gejman, P.V. The sympathetic superior cervical ganglia as peripheral neuroendocrine centers. J. Neural Transmission 52, 1–21 (1981). https://doi.org/10.1007/BF01253092

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01253092

Key words

Search

Navigation