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. 1994 Mar 1;91(5):1761–1765. doi: 10.1073/pnas.91.5.1761

Single-channel currents trigger action potentials in small cultured hippocampal neurons.

S Johansson 1, P Arhem 1
PMCID: PMC43243  PMID: 7510406

Abstract

Spontaneous neuronal impulse activity appears to play a key role in some neural processes, such as the normal establishment of interneuronal connections during development. In addition, spontaneous impulses may be essential for the functional operation of neuronal networks. Mechanisms of spontaneous non-pacemaker impulse generation are, however, not well known. In this work, spontaneous electrical activity in small cultured hippocampal neurons from rat was studied with tight-seal recording techniques. The results demonstrate that spontaneous individual openings of single ion channels can trigger impulse generation in these high-resistance cells. First, impulses recorded in the whole-cell mode were apparently induced by spontaneous plateau-potential events showing the characteristics expected from individual openings and closures of ion channels. Second, patch-clamp recordings in the cell-attached configuration showed that openings of single ion channels in the patch membrane could trigger cellular impulses, detected as biphasic current deflections. These findings suggest that the random gating of ion channel molecules can be used as a mechanism for stochastic triggering of spontaneous impulses in mammalian central neurons.

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Selected References

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  1. Alving B. O. Spontaneous activity in isolated somata of Aplysia pacemaker naurons. J Gen Physiol. 1968 Jan;51(1):29–45. doi: 10.1085/jgp.51.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ashcroft F. M., Harrison D. E., Ashcroft S. J. Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. 1984 Nov 29-Dec 5Nature. 312(5993):446–448. doi: 10.1038/312446a0. [DOI] [PubMed] [Google Scholar]
  3. Barry P. H., Lynch J. W. Liquid junction potentials and small cell effects in patch-clamp analysis. J Membr Biol. 1991 Apr;121(2):101–117. doi: 10.1007/BF01870526. [DOI] [PubMed] [Google Scholar]
  4. Bergey G. K., Fitzgerald S. C., Schrier B. K., Nelson P. G. Neuronal maturation in mammalian cell culture is dependent on spontaneous electrical activity. Brain Res. 1981 Feb 23;207(1):49–58. doi: 10.1016/0006-8993(81)90678-8. [DOI] [PubMed] [Google Scholar]
  5. Berridge M. J., Rapp P. E. A comparative survey of the function, mechanism and control of cellular oscillators. J Exp Biol. 1979 Aug;81:217–279. doi: 10.1242/jeb.81.1.217. [DOI] [PubMed] [Google Scholar]
  6. Buhmann J., Schulten K. Influence of noise on the function of a "physiological" neural network. Biol Cybern. 1987;56(5-6):313–327. doi: 10.1007/BF00319512. [DOI] [PubMed] [Google Scholar]
  7. Chen C. F., Von Baumgarten R., Takeda R. Pacemaker properties of completely isolated neurones in Aplysia californica. Nat New Biol. 1971 Sep 1;233(35):27–29. doi: 10.1038/newbio233027a0. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Fournier E., Crepel F. Electrophysiological properties of dentate granule cells in mouse hippocampal slices maintained in vitro. Brain Res. 1984 Oct 8;311(1):75–86. doi: 10.1016/0006-8993(84)91400-8. [DOI] [PubMed] [Google Scholar]
  10. Frings S., Lindemann B. Odorant response of isolated olfactory receptor cells is blocked by amiloride. J Membr Biol. 1988 Nov;105(3):233–243. doi: 10.1007/BF01871000. [DOI] [PubMed] [Google Scholar]
  11. Galli L., Maffei L. Spontaneous impulse activity of rat retinal ganglion cells in prenatal life. Science. 1988 Oct 7;242(4875):90–91. doi: 10.1126/science.3175637. [DOI] [PubMed] [Google Scholar]
  12. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  13. Hounsgaard J., Kiehn O. Ca++ dependent bistability induced by serotonin in spinal motoneurons. Exp Brain Res. 1985;57(2):422–425. doi: 10.1007/BF00236551. [DOI] [PubMed] [Google Scholar]
  14. Hounsgaard J., Kiehn O. Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J Physiol. 1989 Jul;414:265–282. doi: 10.1113/jphysiol.1989.sp017687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hounsgaard J., Kjaerulff O. Ca2+-Mediated Plateau Potentials in a Subpopulation of Interneurons in the Ventral Horn of the Turtle Spinal Cord. Eur J Neurosci. 1992;4(2):183–188. doi: 10.1111/j.1460-9568.1992.tb00865.x. [DOI] [PubMed] [Google Scholar]
  16. Johansson S., Arhem P. Impulses of variable amplitude recorded from cell-attached patches on small hippocampal neurons. Brain Res. 1992 May 15;580(1-2):185–188. doi: 10.1016/0006-8993(92)90943-4. [DOI] [PubMed] [Google Scholar]
  17. Johansson S., Arhem P. Membrane currents in small cultured rat hippocampal neurons: a voltage-clamp study. J Physiol. 1992 Jan;445:141–156. doi: 10.1113/jphysiol.1992.sp018916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Johansson S., Arhem P. Single K(+)-channel currents under steady-state potential conditions in small hippocampal neurons. Brain Res. 1992 Nov 20;596(1-2):133–141. doi: 10.1016/0006-8993(92)91540-u. [DOI] [PubMed] [Google Scholar]
  19. Johansson S., Friedman W., Arhem P. Impulses and resting membrane properties of small cultured rat hippocampal neurons. J Physiol. 1992 Jan;445:129–140. doi: 10.1113/jphysiol.1992.sp018915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kehl S. J., McBurney R. N. The firing patterns of rat melanotrophs recorded using the patch clamp technique. Neuroscience. 1989;33(3):579–586. doi: 10.1016/0306-4522(89)90410-7. [DOI] [PubMed] [Google Scholar]
  21. Lynch J. W., Barry P. H. Action potentials initiated by single channels opening in a small neuron (rat olfactory receptor). Biophys J. 1989 Apr;55(4):755–768. doi: 10.1016/S0006-3495(89)82874-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. MacVicar B. A., Dudek F. E. Electrotonic coupling between granule cells of rat dentate gyrus: physiological and anatomical evidence. J Neurophysiol. 1982 Apr;47(4):579–592. doi: 10.1152/jn.1982.47.4.579. [DOI] [PubMed] [Google Scholar]
  23. Marder E. Plateaus in time. Curr Biol. 1991 Oct;1(5):326–327. doi: 10.1016/0960-9822(91)90101-2. [DOI] [PubMed] [Google Scholar]
  24. Maue R. A., Dionne V. E. Patch-clamp studies of isolated mouse olfactory receptor neurons. J Gen Physiol. 1987 Jul;90(1):95–125. doi: 10.1085/jgp.90.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nelson P. G., Yu C., Fields R. D., Neale E. A. Synaptic connections in vitro: modulation of number and efficacy by electrical activity. Science. 1989 May 5;244(4904):585–587. doi: 10.1126/science.2717942. [DOI] [PubMed] [Google Scholar]
  26. Ochoa J., Torebjörk E. Sensations evoked by intraneural microstimulation of single mechanoreceptor units innervating the human hand. J Physiol. 1983 Sep;342:633–654. doi: 10.1113/jphysiol.1983.sp014873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Taraskevich P. S., Douglas W. W. Catecholamines of supposed inhibitory hypophysiotrophic function suppress action potentials in prolactin cells. Nature. 1978 Dec 21;276(5690):832–834. doi: 10.1038/276832a0. [DOI] [PubMed] [Google Scholar]
  28. Vallbo A. B., Olsson K. A., Westberg K. G., Clark F. J. Microstimulation of single tactile afferents from the human hand. Sensory attributes related to unit type and properties of receptive fields. Brain. 1984 Sep;107(Pt 3):727–749. doi: 10.1093/brain/107.3.727. [DOI] [PubMed] [Google Scholar]

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