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. 1988 Feb;396:399–415. doi: 10.1113/jphysiol.1988.sp016969

Ionic basis of the differential neuronal activity of guinea-pig septal nucleus studied in vitro.

G Alvarez de Toledo 1, J López-Barneo 1
PMCID: PMC1192052  PMID: 2457690

Abstract

1. The electrical properties and ionic conductances of septal neurones were studied by intracellular recording in an in vitro slice preparation. Within the total number of cells recorded (n = 150) we identified three electrophysiological cell types, each one of them located in a separate septal region. Dorsolateral septal neurones comprised 60% of the cells, intermediate septal neurons 10%, and medical septal neurones 30%. 2. Passive electrical constants of dorsolateral, intermediate and medial septal neurones were, respectively:resting potential (-60.2 +/- 4.8, -59.8 +/- 3.3 and -56 +/- 4.3 mV); input resistance (82.5 +/- 17, 63 +/- 16 and 83 +/- 18 M omega) and membrane time constant (18.5 +/- 7.3, 14.2 +/- 6.8 and 10.7 +/- 3.4 ms). 3. Direct activation of dorsolateral septal neurones by current injection below 0.2 nA triggered repetitive firing of fast action potentials. Larger current pulses elicited a characteristic response consisting of an initial fast action potential followed by a train of slow spikes. An after-hyperpolarization followed termination of the pulse and the characteristic response. 4. In dorsolateral septal neurons tetrodotoxin (TTX) abolished the fast action potentials. The slow spikes and the after-hyperpolarization disappeared in presence of Co2+ or after brief removal of external Ca2+. This suggests that the characteristic response is mediated by Ca2+ and the after-hyperpolarization by a Ca2+-dependent K+ conductance. 5. The firing pattern of intermediate septal neurones activated from the resting potential spontaneously measured in the cells was similar to that of dorsolateral septal neurones; but direct activation from a hyperpolarized membrane potential evoked in intermediate septal cells a bursting response due to the generation of a low-threshold spike. The low-threshold spike was TTX-resistant but abolished by Co2+ and reached a maximal amplitude after hyperpolarization to -75 mV lasting for 100-150 ms. These results suggest the existence in intermediate septal neurons of a low-threshold Ca2+ conductance inactivated at the resting potential and deinactivated by hyperpolarization. 6. Depolarization of medial septal neurons by current pulses of amplitude greater than 0.2-0.3 nA elicited a typical burst of two to six action potentials. The bursts lasted for 20-50 ms and were followed by a marked after-hyperpolarization.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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

  1. ANDY O. J., STEPHAN H. Septal nuclei in the Soricidae (insectivors). Cyto-architectonic study. J Comp Neurol. 1961 Oct;117:251–273. doi: 10.1002/cne.901170211. [DOI] [PubMed] [Google Scholar]
  2. Apostol G., Creutzfeldt O. D. Crosscorrelation between the activity of septal units and hippocampal EEG during arousal. Brain Res. 1974 Feb 15;67(1):65–75. doi: 10.1016/0006-8993(74)90298-4. [DOI] [PubMed] [Google Scholar]
  3. BRUECKE F., PETSCHE H., PILLAT B., DEISENHAMMER E. [The influencing of the "hippocampus arousal reaction" in the rabbit by electrical stimulation in the septum]. Pflugers Arch Gesamte Physiol Menschen Tiere. 1959;269:319–338. [PubMed] [Google Scholar]
  4. Blankenship J. E., Kuno M. Analysis of spontaneous subthreshold activity in spinal motoneurons of the cat. J Neurophysiol. 1968 Mar;31(2):195–209. doi: 10.1152/jn.1968.31.2.195. [DOI] [PubMed] [Google Scholar]
  5. Brown D. A., Constanti A., Adams P. R. Ca-activated potassium current in vertebrate sympathetic neurons. Cell Calcium. 1983 Dec;4(5-6):407–420. doi: 10.1016/0143-4160(83)90017-9. [DOI] [PubMed] [Google Scholar]
  6. Brown T. H., Fricke R. A., Perkel D. H. Passive electrical constants in three classes of hippocampal neurons. J Neurophysiol. 1981 Oct;46(4):812–827. doi: 10.1152/jn.1981.46.4.812. [DOI] [PubMed] [Google Scholar]
  7. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Connors B. W., Gutnick M. J., Prince D. A. Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol. 1982 Dec;48(6):1302–1320. doi: 10.1152/jn.1982.48.6.1302. [DOI] [PubMed] [Google Scholar]
  9. DeFrance J. F., Yoshihara H., Chronister R. B. Electrophysiological studies of the septal nuclei: I. The lateral septal region. Exp Neurol. 1976 Nov;53(2):399–419. doi: 10.1016/0014-4886(76)90081-9. [DOI] [PubMed] [Google Scholar]
  10. Dutar P., Lamour Y., Jobert A. Activation of identified septo-hippocampal neurons by noxious peripheral stimulation. Brain Res. 1985 Feb 25;328(1):15–21. doi: 10.1016/0006-8993(85)91317-4. [DOI] [PubMed] [Google Scholar]
  11. GREEN J. D., ARDUINI A. A. Hippocampal electrical activity in arousal. J Neurophysiol. 1954 Nov;17(6):533–557. doi: 10.1152/jn.1954.17.6.533. [DOI] [PubMed] [Google Scholar]
  12. Galvan M., Sedlmeir C. Outward currents in voltage-clamped rat sympathetic neurones. J Physiol. 1984 Nov;356:115–133. doi: 10.1113/jphysiol.1984.sp015456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gustafsson B., Galvan M., Grafe P., Wigström H. A transient outward current in a mammalian central neurone blocked by 4-aminopyridine. Nature. 1982 Sep 16;299(5880):252–254. doi: 10.1038/299252a0. [DOI] [PubMed] [Google Scholar]
  14. Hagiwara S., Fukuda J., Eaton D. C. Membrane currents carried by Ca, Sr, and Ba in barnacle muscle fiber during voltage clamp. J Gen Physiol. 1974 May;63(5):564–578. doi: 10.1085/jgp.63.5.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jahnsen H., Llinás R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol. 1984 Apr;349:205–226. doi: 10.1113/jphysiol.1984.sp015153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Joëls M., Twery M. J., Shinnick-Gallagher P., Gallagher J. P. Multiple actions of serotonin on lateral septal neurons in rat brain. Eur J Pharmacol. 1986 Sep 23;129(1-2):203–204. doi: 10.1016/0014-2999(86)90357-2. [DOI] [PubMed] [Google Scholar]
  17. Junge D. Calcium dependence of A-currents in perfused Aplysia neurons. Brain Res. 1985 Nov 4;346(2):294–300. doi: 10.1016/0006-8993(85)90863-7. [DOI] [PubMed] [Google Scholar]
  18. Lamour Y., Dutar P., Jobert A. Septo-hippocampal and other medial septum-diagonal band neurons: electrophysiological and pharmacological properties. Brain Res. 1984 Sep 10;309(2):227–239. doi: 10.1016/0006-8993(84)90588-2. [DOI] [PubMed] [Google Scholar]
  19. Lebrun C. J., Poulain D. A. Electrical activity of septal neurones during suckling and the milk ejection reflex in the lactating rat. Exp Brain Res. 1982;47(2):203–208. doi: 10.1007/BF00239379. [DOI] [PubMed] [Google Scholar]
  20. Lebrun C. J., Poulain D. A., Theodosis D. T. The role of the septum in the control of the milk ejection reflex in the rat: effects of lesions and electrical stimulation. J Physiol. 1983 Jun;339:17–31. doi: 10.1113/jphysiol.1983.sp014699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol. 1980 Aug;305:171–195. doi: 10.1113/jphysiol.1980.sp013357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Llinás R., Yarom Y. Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J Physiol. 1981 Jun;315:549–567. doi: 10.1113/jphysiol.1981.sp013763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. López-Barneo J., Alvarez de Toledo G., Yarom Y. Electrophysiological properties of guinea pig septal neurons in vitro. Brain Res. 1985 Nov 18;347(2):358–362. doi: 10.1016/0006-8993(85)90199-4. [DOI] [PubMed] [Google Scholar]
  24. López-Barneo J., Armstrong C. M. Depolarizing response of rat parathyroid cells to divalent cations. J Gen Physiol. 1983 Aug;82(2):269–294. doi: 10.1085/jgp.82.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. MacDermott A. B., Weight F. F. Action potential repolarization may involve a transient, Ca2+-sensitive outward current in a vertebrate neurone. Nature. 1982 Nov 11;300(5888):185–188. doi: 10.1038/300185a0. [DOI] [PubMed] [Google Scholar]
  26. McLennan H., Miller J. J. Frequency-related inhibitory mechanisms controlling rhythmical activity in the septal area. J Physiol. 1976 Jan;254(3):827–841. doi: 10.1113/jphysiol.1976.sp011263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McLennan H., Miller J. J. The hippocampal control of neuronal discharges in the septum of the rat. J Physiol. 1974 Mar;237(3):607–624. doi: 10.1113/jphysiol.1974.sp010500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Meibach R. C., Siegel A. Efferent connections of the septal area in the rat: an analysis utilizing retrograde and anterograde transport methods. Brain Res. 1977 Jan 1;119(1):1–20. doi: 10.1016/0006-8993(77)90088-9. [DOI] [PubMed] [Google Scholar]
  29. Murase K., Randić M. Electrophysiological properties of rat spinal dorsal horn neurones in vitro: calcium-dependent action potentials. J Physiol. 1983 Jan;334:141–153. doi: 10.1113/jphysiol.1983.sp014485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Neher E. Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol. 1971 Jul;58(1):36–53. doi: 10.1085/jgp.58.1.36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. PETSCHE H., GOGOLAK G., VANZWIETEN P. A. RHYTHMICITY OF SEPTAL CELL DISCHARGES AT VARIOUS LEVELS OF RETICULAR EXCITATION. Electroencephalogr Clin Neurophysiol. 1965 Jul;19:25–33. doi: 10.1016/0013-4694(65)90004-0. [DOI] [PubMed] [Google Scholar]
  32. Raisman G. The connexions of the septum. Brain. 1966 Jun;89(2):317–348. doi: 10.1093/brain/89.2.317. [DOI] [PubMed] [Google Scholar]
  33. Schwartzkroin P. A., Slawsky M. Probable calcium spikes in hippocampal neurons. Brain Res. 1977 Oct 21;135(1):157–161. doi: 10.1016/0006-8993(77)91060-5. [DOI] [PubMed] [Google Scholar]
  34. Segal M., Barker J. L. Rat hippocampal neurons in culture: potassium conductances. J Neurophysiol. 1984 Jun;51(6):1409–1433. doi: 10.1152/jn.1984.51.6.1409. [DOI] [PubMed] [Google Scholar]
  35. Stevens D. R., Gallagher J. P., Shinnick-Gallagher P. Intracellular recordings from rat dorsolateral septal neurons, in vitro. Brain Res. 1984 Jul 9;305(2):353–356. doi: 10.1016/0006-8993(84)90441-4. [DOI] [PubMed] [Google Scholar]
  36. Thompson S. H. Three pharmacologically distinct potassium channels in molluscan neurones. J Physiol. 1977 Feb;265(2):465–488. doi: 10.1113/jphysiol.1977.sp011725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vinogradova O. S., Brazhnik E. S., Karanov A. M., Zhadina S. D. Neuronal activity of the septum following various types of deafferentation. Brain Res. 1980 Apr 14;187(2):353–368. doi: 10.1016/0006-8993(80)90208-5. [DOI] [PubMed] [Google Scholar]
  38. Zbicz K. L., Weight F. F. Transient voltage and calcium-dependent outward currents in hippocampal CA3 pyramidal neurons. J Neurophysiol. 1985 Apr;53(4):1038–1058. doi: 10.1152/jn.1985.53.4.1038. [DOI] [PubMed] [Google Scholar]

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