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. 1996 Sep 3;93(18):9905–9909. doi: 10.1073/pnas.93.18.9905

Quantal release at a neuronal nicotinic synapse from rat adrenal gland.

J G Barbara 1, K Takeda 1
PMCID: PMC38527  PMID: 8790429

Abstract

The neuronal nicotinic synapse in tissue slices of the adrenal medulla was studied with whole-cell patch-clamp. Excitatory postsynaptic currents (EPSCs) were evoked by local field stimulation or occurred spontaneously especially when external [K+] was increased. EPSCs were carried by channels sharing biophysical and pharmacological properties of neuronal-type nicotinic receptors (nAChRs). A single-channel conductance (gamma) of 43-45 pS was found from nonstationary variance analysis of EPSCs. Spontaneous EPSCs were tetrodotoxin-insensitive and Ca(2+)-dependent and occurred in burst-like clusters. Quantal analysis of spontaneous EPSCs gave a quantal size of 20 pA and amplitude histograms were well described by binomial models with low values of quantal content, consistent with a small number of spontaneously active release sites. However, rare large amplitude EPSCs suggest that the total number of sites is higher and that extrajunctional receptors are involved. Our estimates of quantal content and size at the chromaffin cell neuronal nicotinic synapse may be useful in characterizing central neuronal-type nicotinic receptor-mediated cholinergic synaptic transmission.

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Selected References

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

  1. BLACKMAN J. G., GINSBORG B. L., RAY C. On the quantal release of the transmitter at a sympathetic synapse. J Physiol. 1963 Jul;167:402–415. doi: 10.1113/jphysiol.1963.sp007158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bekkers J. M., Richerson G. B., Stevens C. F. Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc Natl Acad Sci U S A. 1990 Jul;87(14):5359–5362. doi: 10.1073/pnas.87.14.5359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bornstein J. C. Spontaneous multiquantal release at synapses in guinea-pig hypogastric ganglia: evidence that release can occur in bursts. J Physiol. 1978 Sep;282:375–398. doi: 10.1113/jphysiol.1978.sp012470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brown D. A., Docherty R. J., Halliwell J. V. The action of cholinomimetic substances on impulse conduction in the habenulointerpeduncular pathway of the rat in vitro. J Physiol. 1984 Aug;353:101–109. doi: 10.1113/jphysiol.1984.sp015325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cimino M., Marini P., Fornasari D., Cattabeni F., Clementi F. Distribution of nicotinic receptors in cynomolgus monkey brain and ganglia: localization of alpha 3 subunit mRNA, alpha-bungarotoxin and nicotine binding sites. Neuroscience. 1992 Nov;51(1):77–86. doi: 10.1016/0306-4522(92)90472-e. [DOI] [PubMed] [Google Scholar]
  6. Coupland R. E. Electron microscopic observations on the structure of the rat adrenal medulla: II. Normal innervation. J Anat. 1965 Apr;99(Pt 2):255–272. [PMC free article] [PubMed] [Google Scholar]
  7. Criado M., Alamo L., Navarro A. Primary structure of an agonist binding subunit of the nicotinic acetylcholine receptor from bovine adrenal chromaffin cells. Neurochem Res. 1992 Mar;17(3):281–287. doi: 10.1007/BF00966671. [DOI] [PubMed] [Google Scholar]
  8. De Koninck Y., Mody I. Noise analysis of miniature IPSCs in adult rat brain slices: properties and modulation of synaptic GABAA receptor channels. J Neurophysiol. 1994 Apr;71(4):1318–1335. doi: 10.1152/jn.1994.71.4.1318. [DOI] [PubMed] [Google Scholar]
  9. Derkach V. A., Selyanko A. A., Skok V. I. Acetylcholine-induced current fluctuations and fast excitatory post-synaptic currents in rabbit sympathetic neurones. J Physiol. 1983 Mar;336:511–526. doi: 10.1113/jphysiol.1983.sp014595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. ECCLES J. C., FATT P., KOKETSU K. Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol. 1954 Dec 10;126(3):524–562. doi: 10.1113/jphysiol.1954.sp005226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Edwards F. A., Konnerth A., Sakmann B. Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J Physiol. 1990 Nov;430:213–249. doi: 10.1113/jphysiol.1990.sp018289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Egan T. M., North R. A. Actions of acetylcholine and nicotine on rat locus coeruleus neurons in vitro. Neuroscience. 1986 Oct;19(2):565–571. doi: 10.1016/0306-4522(86)90281-2. [DOI] [PubMed] [Google Scholar]
  13. Fenwick E. M., Marty A., Neher E. A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. J Physiol. 1982 Oct;331:577–597. doi: 10.1113/jphysiol.1982.sp014393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hessler N. A., Shirke A. M., Malinow R. The probability of transmitter release at a mammalian central synapse. Nature. 1993 Dec 9;366(6455):569–572. doi: 10.1038/366569a0. [DOI] [PubMed] [Google Scholar]
  15. Hirst G. D., McLachlan E. M. Post-natal development of ganglia in the lower lumbar sympathetic chain of the rat. J Physiol. 1984 Apr;349:119–134. doi: 10.1113/jphysiol.1984.sp015147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Holman M. E., Coleman H. A., Tonta M. A., Parkington H. C. Synaptic transmission from splanchnic nerves to the adrenal medulla of guinea-pigs. J Physiol. 1994 Jul 1;478(Pt 1):115–124. doi: 10.1113/jphysiol.1994.sp020235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Holman M. E., Tonta M. A., Coleman H. A., Parkington H. C. Currents caused by the spontaneous release of quanta of acetylcholine onto chromaffin cells in guinea-pig adrenal medulla. Neurosci Lett. 1995 Jan 23;184(2):75–78. doi: 10.1016/0304-3940(94)11172-f. [DOI] [PubMed] [Google Scholar]
  18. Jonas P., Major G., Sakmann B. Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol. 1993 Dec;472:615–663. doi: 10.1113/jphysiol.1993.sp019965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Korn H., Faber D. S. Quantal analysis and synaptic efficacy in the CNS. Trends Neurosci. 1991 Oct;14(10):439–445. doi: 10.1016/0166-2236(91)90042-s. [DOI] [PubMed] [Google Scholar]
  20. Kullmann D. M., Nicoll R. A. Long-term potentiation is associated with increases in quantal content and quantal amplitude. Nature. 1992 May 21;357(6375):240–244. doi: 10.1038/357240a0. [DOI] [PubMed] [Google Scholar]
  21. Luetje C. W., Patrick J., Séguéla P. Nicotine receptors in the mammalian brain. FASEB J. 1990 Jul;4(10):2753–2760. doi: 10.1096/fasebj.4.10.2197155. [DOI] [PubMed] [Google Scholar]
  22. Léna C., Changeux J. P., Mulle C. Evidence for "preterminal" nicotinic receptors on GABAergic axons in the rat interpeduncular nucleus. J Neurosci. 1993 Jun;13(6):2680–2688. doi: 10.1523/JNEUROSCI.13-06-02680.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. MARTIN A. R., PILAR G. QUANTAL COMPONENTS OF THE SYNAPTIC POTENTIAL IN THE CILIARY GANGLION OF THE CHICK. J Physiol. 1964 Dec;175:1–16. doi: 10.1113/jphysiol.1964.sp007499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maconochie D. J., Knight D. E. A study of the bovine adrenal chromaffin nicotinic receptor using patch clamp and concentration-jump techniques. J Physiol. 1992 Aug;454:129–153. doi: 10.1113/jphysiol.1992.sp019257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Malinow R. Transmission between pairs of hippocampal slice neurons: quantal levels, oscillations, and LTP. Science. 1991 May 3;252(5006):722–724. doi: 10.1126/science.1850871. [DOI] [PubMed] [Google Scholar]
  26. McCormick D. A., Prince D. A. Acetylcholine causes rapid nicotinic excitation in the medial habenular nucleus of guinea pig, in vitro. J Neurosci. 1987 Mar;7(3):742–752. doi: 10.1523/JNEUROSCI.07-03-00742.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McGehee D. S., Role L. W. Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu Rev Physiol. 1995;57:521–546. doi: 10.1146/annurev.ph.57.030195.002513. [DOI] [PubMed] [Google Scholar]
  28. Nooney J. M., Feltz A. Inhibition by cyclothiazide of neuronal nicotinic responses in bovine chromaffin cells. Br J Pharmacol. 1995 Feb;114(3):648–655. doi: 10.1111/j.1476-5381.1995.tb17188.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nooney J. M., Lambert J. J., Chiappinelli V. A. The interaction of kappa-bungarotoxin with the nicotinic receptor of bovine chromaffin cells. Brain Res. 1992 Feb 21;573(1):77–82. doi: 10.1016/0006-8993(92)90115-p. [DOI] [PubMed] [Google Scholar]
  30. Paulsen O., Heggelund P. The quantal size at retinogeniculate synapses determined from spontaneous and evoked EPSCs in guinea-pig thalamic slices. J Physiol. 1994 Nov 1;480(Pt 3):505–511. doi: 10.1113/jphysiol.1994.sp020379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rang H. P. The characteristics of synaptic currents and responses to acetylcholine of rat submandibular ganglion cells. J Physiol. 1981 Feb;311:23–55. doi: 10.1113/jphysiol.1981.sp013571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Redman S. Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol Rev. 1990 Jan;70(1):165–198. doi: 10.1152/physrev.1990.70.1.165. [DOI] [PubMed] [Google Scholar]
  33. Ropert N., Miles R., Korn H. Characteristics of miniature inhibitory postsynaptic currents in CA1 pyramidal neurones of rat hippocampus. J Physiol. 1990 Sep;428:707–722. doi: 10.1113/jphysiol.1990.sp018236. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rosenmund C., Clements J. D., Westbrook G. L. Nonuniform probability of glutamate release at a hippocampal synapse. Science. 1993 Oct 29;262(5134):754–757. doi: 10.1126/science.7901909. [DOI] [PubMed] [Google Scholar]
  35. Vidal C., Changeux J. P. Pharmacological profile of nicotinic acetylcholine receptors in the rat prefrontal cortex: an electrophysiological study in a slice preparation. Neuroscience. 1989;29(2):261–270. doi: 10.1016/0306-4522(89)90056-0. [DOI] [PubMed] [Google Scholar]
  36. Wong L. A., Gallagher J. P. A direct nicotinic receptor-mediated inhibition recorded intracellularly in vitro. Nature. 1989 Oct 5;341(6241):439–442. doi: 10.1038/341439a0. [DOI] [PubMed] [Google Scholar]
  37. Zhou Z., Misler S. Action potential-induced quantal secretion of catecholamines from rat adrenal chromaffin cells. J Biol Chem. 1995 Feb 24;270(8):3498–3505. [PubMed] [Google Scholar]
  38. Zhou Z., Neher E. Calcium permeability of nicotinic acetylcholine receptor channels in bovine adrenal chromaffin cells. Pflugers Arch. 1993 Dec;425(5-6):511–517. doi: 10.1007/BF00374879. [DOI] [PubMed] [Google Scholar]

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