Skip to main content
NCBI home page
Cellular and Molecular Neurobiology logoLink to Cellular and Molecular Neurobiology
. 1987 Jun;7(2):175–189. doi: 10.1007/BF00711553

Properties of miniature postsynaptic currents during depolarization-induced release at a cholinergic neuroneuronal synapse

M Simonneau 1, L Tauc 1
PMCID: PMC11567417  PMID: 3652114

Abstract

  1. Miniature postsynaptic currents were analyzed at an inhibitory cholinergic neuroneuronal synapse in the buccal ganglion ofAplysia. Under double voltage-clamp, it was possible to induce postsynaptic currents by long-duration depolarizations of the presynaptic neuron and to analyze these as the linear summation of individual miniature postsynaptic currents (MPSCs). The amplitude of these miniature currents (i min) was calculated from the ratio of the variance of the noise (E 2) to the mean of the postsynaptic current (I m), according to Campbell's theorem, withi min = 2E 2/I m. Their decay time (τ min) was obtained from the cutoff frequencies of the power spectra obtained from the noise.

  2. Neither the conductance nor the decay time of MPSCs was voltage dependent. However,i min appeared to decrease when the quantal content of the response increased. Meanwhile,τ min increased slightly withI min.

  3. Carbamylcholine was injected into the neuropile and this led to a decrease ini min and a slight increase inτ min.

  4. Power spectra obtained after the application of inhibitors of acetylcholinesterase (AChE), with or without curare, suggested that acetylcholine (ACh) does not accumulate during large depolarizations.

  5. The possible origin of the nonlinear relationship between the variance and the mean of the postsynaptic currents is discussed.

Key words: cholinergic neuroneuronal synapse, Aplysia californica, miniature postsynaptic currents

References

  1. Adams, D. J., Gage, P. W., and Hamill, O. P. (1976). Voltage sensitivity of inhibitory postsynaptic currents inAplysia buccal ganglia.Brain Res.115:506–511. [DOI] [PubMed] [Google Scholar]
  2. Auerbach, A. A., and Bennett, M. V. L. (1969). Chemically mediated transmission at a giant fiber synapse in the central nervous system of a vertebrate.J. Physiol.53:183–210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barrantes, F. J., Sakmann, B., Bonner, R., Eirl, H., and Jovin, T. M. (1975). 1-Pyrene butylcholine: A fluorescent probe for the cholinergic system.Proc. Natl. Acad. Sci. USA72:3097–3101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baux, G., Simonneau, M., and Tauc, L. (1979). Transmitter release: Ruthenium red used to demonstrate a possible role of sialic acid containing substrates.J. Physiol.291:161–178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bullock, T. H. (1948). Properties of a single synapse in the stellate ganglion of squid.J. Neurophysiol.11:343–364. [DOI] [PubMed] [Google Scholar]
  6. Colquhoun, D. (1979). The link between drug binding and response: Theories and observations. InReceptors, A Comprehensive Treatise (R. D. O'Brien, Ed.), Plenum Press, New York, Vol. 1, pp. 93–142. [Google Scholar]
  7. Colquhoun, D., Large, W. A., and Rang, H. P. (1977). An analysis of the action of a false transmitter at the neuro-muscular junction.J. Physiol.266:361–395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Couraud, J. Y. (1974).Etude de la Libération du Médiateur Après Injection Intracellulaire de Produits Radioactifs dans les Neurones d'Aplysia, D.E.A., Paris VI. [Google Scholar]
  9. Cull-Candy, S. G., Miledi, R., and Uchitel, O. D. (1980). Diffusion of acetylcholine in the synaptic cleft of normal and myasthenia gravis human endplates.Nature286:500–502. [DOI] [PubMed] [Google Scholar]
  10. Dunant, Y., Eder, L., and Hirt, L. S. (1980). Acetylcholine release evoked by a single or few nerve impulses in the electric organs ofTorpedo.J. Physiol.298:185–203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Feltz, A., and Trautmann, A. (1980). Interaction between nerve-released acetylcholine and bath applied agonists at the frog end-plate.J. Physiol.299:533–552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fiekers, J. F. (1985). Concentration-dependent effects of neostigmine on the endplate acetylcholine receptor channel complex.J. Neurosci.5:502–514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gage, P. W. (1976). Generation of end-plate potentials.Physiol. Rev.56:177–247. [DOI] [PubMed] [Google Scholar]
  14. Gardner, D. (1971). Bilateral symmetry and interneuronal organization in the buccal ganglion of Aplysia.Science173:550–553. [DOI] [PubMed] [Google Scholar]
  15. Gardner, D., and Stevens, C. F. (1980). Rate-limiting step of inhibitory postsynaptic decay inAplysia buccal ganglia.J. Physiol.304:145–164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hartzell, H. C., Kuffler, S. W., and Yoshikami, D. (1975). Postsynaptic potentiation: Interaction between quanta of acetylcholine at the skeletal neuromuscular synapse.J. Physiol.251:427–463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Katz, B., and Miledi, R. (1972). The statistical nature of the acetylcholine potential and its molecular components.J. Physiol.224:665–699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Katz, B., and Miledi, R. (1973). The binding of acetylcholine to receptors and its removal from the synaptic cleft.J. Physiol.231:549–574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Katz, B., and Miledi, R. (1977). Transmitter leakage from motor nerve endings.Proc. Roy. Soc. Lond. B196:59–72. [DOI] [PubMed] [Google Scholar]
  20. Llinas, R., Joyner, R. W., and Nicholson, C. (1974). Equilibrium potential for the postsynaptic response in the squid giant synapse.J. Gen. Physiol.64:519–535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Llinas, R., Steinberg, I. Z., and Walton, K. (1981a). Presynaptic calcium currents in squid giant synapse.Biophys. J.33:289–322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Llinas, R., Steinberg, I. Z., and Walton, K. (1981b). Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse.Biophys. J.33:323–352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Magleby, K. L., and Stevens, C. F. (1972). A quantitative description of end-plate currents.J. Physiol.233:173–197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Martin, A. R., and Ringham, G. L. (1975). Synaptic transfer at a vertebrate central nervous system synapse.J. Physiol.251:409–426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nicholls, J., and Wallace, B. G. (1978a). Modulation of transmission at an inhibitory synapse in the central nervous system of the leech.J. Physiol.281:157–170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nicholls, J., and Wallace, B. G. (1978b). Quantal analysis of transmitter release at an inhibitory synapse in the central nervous system of the leech.J. Physiol.281:171–185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Poo, M. M., Sun, Y. A., and Young, S. H. (1985). Three types of transmitter release from embryonic neurons.J. Physiol. (Paris)80:283–289. [PubMed] [Google Scholar]
  28. Sigworth, F. J. (1980). The variance of sodium current fluctuations at the node of Ranvier.J. Physiol.307:97–129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Simon, S. M., and Llinas, R. R. (1985). Compartmentalization of the submembrane calcium activity during calcium current and postsynaptic potential in squid giant synapse.Biophys. J.48:323–352. [Google Scholar]
  30. Simonneau, M., and Tauc, L. (1981). Introduction of substances into cells: Iontophoresis. InTechniques in Cellular Physiology (P. F. Baker, Ed.), Elsevier, New York, pp. 1–15. [Google Scholar]
  31. Simonneau, M., Baux, G., and Tauc, L. (1980a). Quantal analysis of transmitter release at an identified synapse. InOntogenesis and Functional Mechanisms of Peripheral Synapses (Taxi, Ed.), Elsevier, Amsterdam, pp. 179–189. [Google Scholar]
  32. Simonneau, M., Tauc, L., and Baux, G. (1980b). Quantal release of acetylcholine examined by a current fluctuation analysis at an identified neuro-neuronal synapse ofAplysia.Proc. Natl. Acad. Sci. USA77:1661–1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sun, Y. A., and Poo, M. M. (1985). Non-quantal release of acetylcholine at a developing neuromuscular junction.J. Neurosci.5:634–642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Van Helden, D. F., Gage, P. W., and Hamill, O. P. (1979). Conductance of end-plate channels is voltage-dependent.Neurosci. Lett.11:227–232. [DOI] [PubMed] [Google Scholar]
  35. Vizi, E. S., and Vyskocil, F. (1979). Changes in total and quantal release of acetylcholine in the mouse diaphragm during activation and inhibition of membrane ATPase.J. Physiol.286:1–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vyskocil, F., Nikolsky, E., and Edwards, C. (1983). An analysis of the mechanism underlying the non-quantal release of acetylcholine at the mouse neuro-muscular junction.Neuroscience9:429–435. [DOI] [PubMed] [Google Scholar]
  37. White, R. L., and Gardner, D. (1983). Physostygmine prolongs the elementary events underlying decay of inhibitory post-synaptic currents in Aplysia.J. Neurosci.3:2607–2613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Young, S. H., and Poo, M. M. (1983). Spontaneous release of transmitter from growth cones of embryonic neurones.Nature305:634–637. [DOI] [PubMed] [Google Scholar]

Articles from Cellular and Molecular Neurobiology are provided here courtesy of Springer

RESOURCES