Skip to main content
NCBI home page
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
. 1974 Sep;71(9):3602–3606. doi: 10.1073/pnas.71.9.3602

Evidence for Cholinergic Synapses Between Dissociated Rat Sympathetic Neurons in Cell Culture

P H O'Lague 1, K Obata 1,*, P Claude 1, E J Furshpan 1, D D Potter 1
PMCID: PMC433823  PMID: 4372629

Abstract

Sympathetic principal neurons were dissociated from superior cervical ganglia of new-born rats, and grown in cell culture. In electrophysiological experiments two types of excitatory synapses were found. One, which was relatively rare, was shown to operate by electrical transmission. The other, the predominant type, had several characteristics of chemical transmission, and pharmacological evidence indicated it was cholinergic.

Keywords: synaptic transmitters, neuronal development, cell interaction, ganglionic blocking drugs

Full text

PDF
3602

Images in this article

3603Image
on p.3603
3604Image
on p.3604

Selected References

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

  1. Aiken J. W., Reit E. A comparison of the sensitivity to chemical stimuli of adrenergic and cholinergic neurons in the cat stellate ganglion. J Pharmacol Exp Ther. 1969 Oct;169(2):211–223. [PubMed] [Google Scholar]
  2. BURN J. H., RAND M. J. ACETYLCHOLINE IN ADRENERGIC TRANSMISSION. Annu Rev Pharmacol. 1965;5:163–182. doi: 10.1146/annurev.pa.05.040165.001115. [DOI] [PubMed] [Google Scholar]
  3. Beránek R., Vyskocil F. The action of tubocurarine and atropine on the normal and denervated rat diaphragm. J Physiol. 1967 Jan;188(1):53–66. doi: 10.1113/jphysiol.1967.sp008123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bray D. Surface movements during the growth of single explanted neurons. Proc Natl Acad Sci U S A. 1970 Apr;65(4):905–910. doi: 10.1073/pnas.65.4.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Christ D. D., Nishi S. Effects of adrenaline on nerve terminals in the superior cervical ganglion of the rabbit. Br J Pharmacol. 1971 Feb;41(2):331–338. doi: 10.1111/j.1476-5381.1971.tb08033.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crain S. M., Peterson E. R. Development of neural connections in culture. Ann N Y Acad Sci. 1974 Mar 22;228(0):6–34. doi: 10.1111/j.1749-6632.1974.tb20499.x. [DOI] [PubMed] [Google Scholar]
  7. Dunant Y. Some properties of the presynaptic nerve terminals in a mammalian sympathetic ganglion. J Physiol. 1972 Mar;221(3):577–587. doi: 10.1113/jphysiol.1972.sp009768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. ECCLES R. M., LIBET B. Origin and blockade of the synaptic responses of curarized sympathetic ganglia. J Physiol. 1961 Aug;157:484–503. doi: 10.1113/jphysiol.1961.sp006738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Elfvin L. G. Ultrastructural studies on the synaptology of the inferior mesenteric ganglion of the cat. 3. The structure and distribution of the axodendritic and dendrodendritic contacts. J Ultrastruct Res. 1971 Nov;37(3):432–448. doi: 10.1016/s0022-5320(71)80137-5. [DOI] [PubMed] [Google Scholar]
  10. Elfvin L. G. Ultrastructural studies on the synaptology of the inferior mesenteric ganglion of the cat. I. Observations on the cell surface of the postganglionic perikarya. J Ultrastruct Res. 1971 Nov;37(3):411–425. doi: 10.1016/s0022-5320(71)80135-1. [DOI] [PubMed] [Google Scholar]
  11. Ferry C. B. Cholinergic link hypothesis in adrenergic neuroeffector transmission. Physiol Rev. 1966 Jul;46(3):420–456. doi: 10.1152/physrev.1966.46.3.420. [DOI] [PubMed] [Google Scholar]
  12. Fischbach G. D., Fambrough D., Nelson P. G. A discussion of neuron and muscle cell cultures. Fed Proc. 1973 Jun;32(6):1636–1642. [PubMed] [Google Scholar]
  13. Fischbach G. D. Synapse formation between dissociated nerve and muscle cells in low density cell cultures. Dev Biol. 1972 Jun;28(2):407–429. doi: 10.1016/0012-1606(72)90023-1. [DOI] [PubMed] [Google Scholar]
  14. Grillo M. A. Electron microscopy of sympathetic tissues. Pharmacol Rev. 1966 Mar;18(1):387–399. [PubMed] [Google Scholar]
  15. Jacobowitz D. M., Greene L. A. Histofluorescence study of chromaffin cells in dissociated cell cultures of chick embryo sympathetic ganglia. J Neurobiol. 1974;5(1):65–83. doi: 10.1002/neu.480050107. [DOI] [PubMed] [Google Scholar]
  16. Jacobowitz D. Catecholamine fluorescence studies of adrenergic neurons and chromaffin cells in sympathetic ganglia. Fed Proc. 1970 Nov-Dec;29(6):1929–1944. [PubMed] [Google Scholar]
  17. Klingman G. I. The distribution of acetylcholinesterase in sympathetic ganglia of immunosympathectomized rats. J Pharmacol Exp Ther. 1970 May;173(1):205–211. [PubMed] [Google Scholar]
  18. Kobayashi H., Libet B. Actions of noradrenaline and acetylcholine on sympathetic ganglion cells. J Physiol. 1970 Jun;208(2):353–372. doi: 10.1113/jphysiol.1970.sp009125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. LEVI-MONTALCINI R., ANGELETTI P. U. Essential role of the nerve growth factor in the survival and maintenance of dissociated sensory and sympathetic embryonic nerve cells in vitro. Dev Biol. 1963 Mar;6:653–659. doi: 10.1016/0012-1606(63)90149-0. [DOI] [PubMed] [Google Scholar]
  20. Libet B., Tosaka T. Slow inhibitory and excitatory postsynaptic responses in single cells of mammalian sympathetic ganglia. J Neurophysiol. 1969 Jan;32(1):43–50. doi: 10.1152/jn.1969.32.1.43. [DOI] [PubMed] [Google Scholar]
  21. MURRAY J. G., THOMPSON J. W. The occurrence and function of collateral sprouting in the sympathetic nervous system of the cat. J Physiol. 1957 Jan 23;135(1):133–162. doi: 10.1113/jphysiol.1957.sp005700. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mains R. E., Patterson P. H. Primary cultures of dissociated sympathetic neurons. I. Establishment of long-term growth in culture and studies of differentiated properties. J Cell Biol. 1973 Nov;59(2 Pt 1):329–345. doi: 10.1083/jcb.59.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McAfee D. A., Greengard P. Adenosine 3',5'-monophosphate: electrophysiological evidence for a role in synaptic transmission. Science. 1972 Oct;178(58):310–312. doi: 10.1126/science.178.4058.310. [DOI] [PubMed] [Google Scholar]
  24. McLachlan E. M. The formation of synapses in mammalian sympathetic ganglia reinnervated with preganglionic or somatic nerves. J Physiol. 1974 Feb;237(1):217–242. doi: 10.1113/jphysiol.1974.sp010479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Obata K. Transmitter sensitivities of some nerve and muscle cells in culture. Brain Res. 1974 Jun 14;73(1):71–88. doi: 10.1016/0006-8993(74)91008-7. [DOI] [PubMed] [Google Scholar]
  26. Patterson P. H., Chun L. L. The influence of non-neuronal cells on catecholamine and acetylcholine synthesis and accumulation in cultures of dissociated sympathetic neurons. Proc Natl Acad Sci U S A. 1974 Sep;71(9):3607–3610. doi: 10.1073/pnas.71.9.3607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Peacock J. H., Nelson P. G., Goldstone M. W. Electrophysiologic study of cultured neurons dissociated from spinal cords and dorsal root ganglia of fetal mice. Dev Biol. 1973 Jan;30(1):137–152. doi: 10.1016/0012-1606(73)90053-5. [DOI] [PubMed] [Google Scholar]
  28. Perri V., Sacchi O., Casella C. Synaptically mediated potentials elicited by the stimulation of post-ganglionic trunks in the guinea-pig superior cervical ganglion. Pflugers Arch. 1970;314(1):55–67. doi: 10.1007/BF00587046. [DOI] [PubMed] [Google Scholar]
  29. Robbins N., Yonezawa T. Physiological studies during formation and development of rat neuromuscular junctions in tissue culture. J Gen Physiol. 1971 Oct;58(4):467–481. doi: 10.1085/jgp.58.4.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Taxi J., Gautron J., L'Hermite P. Données ultrastructurales sur une éventuelle modulation adrénergique de l'activité du ganglion cervical supérieur du rat. C R Acad Sci Hebd Seances Acad Sci D. 1969 Oct;269(14):1281–1284. [PubMed] [Google Scholar]
  31. Teichberg S., Holtzman E. Axonal agranular reticulum and synaptic vesicles in cultured embryonic chick sympathetic neurons. J Cell Biol. 1973 Apr;57(1):88–108. doi: 10.1083/jcb.57.1.88. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tranzer J. P., Thoenen H. Electronmicroscopic localization of 5-hydroxydopamine (3,4,5-trihydroxy-phenyl-ethylamine), a new 'false' sympathetic transmitter. Experientia. 1967 Sep 15;23(9):743–745. doi: 10.1007/BF02154151. [DOI] [PubMed] [Google Scholar]
  33. Volle R. L., Hancock J. C. Transmission in sympathetic ganglia. Fed Proc. 1970 Nov-Dec;29(6):1913–1918. [PubMed] [Google Scholar]
  34. Yamauchi A., Lever J. D. Correlations between formol fluorescence and acetylcholinesterase (AChE) staining in the superior cervical ganglion of normal rat, pig and sheep. J Anat. 1971 Dec;110(Pt 3):435–443. [PMC free article] [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