Skip to main content
SpringerLink
Log in

Electrophysiological properties of neurones in cultures from postnatal rat dentate gyrus

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Electrophysiological properties of neurofilament-positive neurones in dissociated cell cultures were prepared at postnatal days 4–5 from rat dentate gyrus and studied using the whole-cell patch-clamp technique. These cells expressed a fast-inactivating, 0.5 μM tetrodotoxin-sensitive Na+ current; a high-voltage-activated (HVA) Ca2+ current, which was 30 μM Cd2+- and partially 2 μM nicardipine-sensitive; and an inward rectifier current, which was sensitive to extracellularly applied 1 mM Cs+. The outward current pattern was composed of a delayed rectifier-like outward current sensitive to 20 mM tetraethylammonium (TEA) and a fast-inactivating, Ca2+-dependent outward current. This transient Ca2+-dependent K+ outward current was identified by a subtraction procedure. K+ currents recorded under conditions of blocked Ca2+ currents (after rundown of the HVA Ca2+ current or blocked by extracellularly applied Cd2+) were subtracted from control currents. By comparison with the current pattern of identified dentate granule cells, it is concluded that the investigated cell type originated from interneurones or projection neurones of the dentate hilus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bean BP (1989) Classes of calcium channels in vertebrate cells. Annu Rev Physiol 51: 367–384

    Google Scholar 

  • Beck H, Ficker E, Heinemann U (1992) Properties of two voltageactivated potassium currents in acutely isolated juvenile rat dentate gyrus granule cells. J Neurophysiol 68: 2086–2099

    Google Scholar 

  • Boss BD, Gozes I, Cowan WM (1987) The survival of dentate gyrus neurons in dissociated culture. Dev Brain Res 36: 199–218

    Google Scholar 

  • Carbone E, Lux HD (1984) A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature 310: 501–503

    Google Scholar 

  • Catterall WA (1992) Cellular and molecular biology of voltagegated sodium channels. Physiol Rev [Suppl] 72: S15-S48

    Google Scholar 

  • Connor JA, Stevens CF (1971) Voltage clamp studies of a transient outward current in gastropod neural somata. J Physiol (Lond) 213: 21–30

    Google Scholar 

  • Conrad CD, Roy EJ (1993) Selective loss of hippocampal granule cells following adrenalectomy: implications for spatial memory. J Neurosci 13: 2582–2590

    Google Scholar 

  • Constanti A, Galvan M (1983) Fast inward-rectifying current accounts for anomalous rectification in olfactory cortex neurones. J Physiol (Lond) 335: 153–178

    Google Scholar 

  • Crain BJ, Westerkam WD, Harrison AH, Nadler JV (1988) Selective neuronal death after transient forebrain ischemia in the Mongolian gerbil: a silver impregnation study. Neuroscience 27: 387–402

    Google Scholar 

  • Cull-Candy SG, Marshall CG, Ogden D (1989) Voltage-activated membrane currents in rat cerebellar granule neurons. J Physiol (Lond) 414: 179–199

    Google Scholar 

  • Ficker E, Heinemann U (1992) Slow and fast transient potassium currents in cultured rat hippocampal cells. J Physiol (Lond) 445: 431–455

    Google Scholar 

  • Fisher RE, Gray R, Johnston D (1990) Properties and distribution of single voltage-gated calcium channels in adult hippocampal neurons. J Neurophysiol 64: 91–104

    Google Scholar 

  • Fox AP, Nowycky MC, Tsien RW (1987) Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol (Lond) 394: 149–172

    Google Scholar 

  • Goodman JH, Wasterlain CG, Massarweh WF, Dean E, Sollas AL, Sloviter RS (1993) Calbindin-D28k immunoreactivity and selective vulnerability to ischemia in the dentate gyrus of the developing rat. Brain Res 606: 309–314

    Google Scholar 

  • Haas KZ, Sperber EF, Moshé SL (1990) Kindling in developing animals: expression of severe seizures and enhanced development of bilateral foci. Dev Brain Res 56: 275–280

    Google Scholar 

  • Halliwell JV, Adams PR (1982) Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250: 71–92

    Google Scholar 

  • He X-P, Lee PHK, Pennypacker KR, Tuominen RK, Mar E-C, Thai L, Hong J-S (1992) Characterization of dynorphin-containing neurons on dissociated dentate gyrus cell cultures. Brain Res 594: 91–98

    Google Scholar 

  • Heinemann U, Beck H, Dreier JP, Ficker E, Stabel J, Zhang CL (1992) The dentate gyrus as a regulated gate for the propagation of epileptiform activity. In: Ribak CE, Gall CM, Mody I (eds) The dentate gyrus and its role in seizures. Elsevier Science, Amsterdam, pp 273–280

    Google Scholar 

  • Hockberger PE, Tseng H-Y, Connor JA (1987) Immunocytochemical and electrophysiological differentiation of rat cerebellar granule cells in explant cultures. J Neurosci 7: 1370–1383

    Google Scholar 

  • Hoehn K, Watson TWJ, MacVicar BA (1993) A novel tetrodotoxin-insensitive, slow sodium current in striatal and hippocampal neurons. Neuron 10: 543–552

    Google Scholar 

  • Huguenard JR, Hamill OP, Prince DA (1988) Developmental Changes in Na+ Conductances in rat neocortical neurons: appearance of a slowly inactivating component. J Neurophysiol 59: 778–795

    Google Scholar 

  • Ikemoto Y, Ono K, Yoshida A, Akaike N (1989) Delayed activation of large-conductance Ca2+-activated K channels in hippocampal neurons of the rat. Biophys J 56: 207–212

    Google Scholar 

  • Kay AR (1991) Inactivation kinetics of calcium current of acutely dissociated CA1 pyramidal cells of the mature guinea-pig hippocampus. J Physiol (Lond) 437: 27–48

    Google Scholar 

  • Köhr G, Mody I (1991) Endogenous intracellular calcium buffering and the activation/inactivation of HVA calcium currents in rat dentate gyrus granule cells. J Gen Physiol 98: 941–967

    Google Scholar 

  • MacDermott AB, Weight FF (1982) Action potential repolarization may involve a transient, Ca2+-sensitive outward current in a vertebrate neurone. Nature 300: 185–188

    Google Scholar 

  • McCormick DA, Pape H-C (1990) Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol (Lond) 431: 291–318

    Google Scholar 

  • McNaughton BL, Barnes CA, Meltzer J, Sutherland RJ (1989) Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp Brain Res 76: 485–496

    Google Scholar 

  • Mintz IM, Venema VJ, Swiderek KM, Lee TD, Bean BP, Adams ME (1992) P-type calcium channels blocked by the spider toxin omega-Aga-IVA. Nature 355: 827–829

    Google Scholar 

  • Mogul DJ, Fox AP (1991) Evidence for multiple types of Ca2+channels in acutely isolated hippocampal CA3 neurones of the guinea-pig. J Physiol (Lond) 433: 259–281

    Google Scholar 

  • Müller W, Lux HD (1993) Analysis of voltage-dependent membrane currents in spatially extended neurons from point-clamp data. J Neurophysiol 69: 241–247

    Google Scholar 

  • Müller W, Misgeld U (1990) Inhibitory role of dentate hilus neurons in guinea pig hippocampal slice. J Neurophysiol 64: 46–56

    Google Scholar 

  • Müller TH, Misgeld U, Swandulla D (1992) Ionic currents in cultured rat hypothalamic neurones. J Physiol (Lond) 450: 41–362

    Google Scholar 

  • Neely A, Lingle CJ (1992) Two components of calcium-activated potassium current in rat adrenal chromaffin cells. J Physiol (Lond) 453: 97–131

    Google Scholar 

  • Neher E (1971) Two fast transient current components during voltage clamp on snail neurons. J Gen Physiol 58: 36–53

    Google Scholar 

  • Ogata N, Tatebayashi H (1990) Sodium current kinetics in freshly isolated neostriatal neurones of the adult guinea pig. Pflugers Arch 416: 594–603

    Google Scholar 

  • Ozawa S, Tsuzuki K, Iino M, Ogura A, Kudo Y (1989) Three types of voltage-dependent calcium current in cultured rat hippocampal neurons. Brain Res 495: 329–336

    Google Scholar 

  • Park CC, Ahmed Z (1991) Characterization of sodium current in developing rat diencephalic neurons in serum-free culture. J Neurophysiol 65: 1011–1021

    Google Scholar 

  • Pun RYK, Behbehani MM (1990) A rapidly inactivating Ca2+-dependent K+ current in pheochromocytoma cells (PC12) of the rat. Pflugers Arch 415: 425–432

    Google Scholar 

  • Rogawski MA (1985) The A-current: how ubiquitous a feature of excitable cells is it? Trends Neurosci 5: 214–219

    Google Scholar 

  • Rudy B (1988) Diversity and ubiquity of K channels. Neuroscience 25: 729–749

    Google Scholar 

  • Sah P, Gibb AJ, Gage PW (1988) The sodium current underlying action potentials in guinea pig hippocampal CA1 neurons. J Gen Physiol 91: 373–398

    Google Scholar 

  • Scharfman HE, Schwartzkroin PA (1988) Electrophysiology of morphologically identified mossy cells of the dentate hilus recorded in guinea pig hippocampal slices. J Neurosci 8: 3812–3821

    Google Scholar 

  • Scharfman HE, Kunkel DD, Schwartzkroin PA (1990) Synaptic connections of dentate granule cells and hilar neurons: results of paired intracellular recordings and intracellular horseradish peroxidase injections. Neuroscience 37: 693–707

    Google Scholar 

  • Sloviter RS (1983) “Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies. Brain Res Bull 10: 675–697

    Google Scholar 

  • Sloviter RS (1987) Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235: 73–76

    Google Scholar 

  • Sloviter RS (1989) Calcium-binding protein (calbindin-d28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280: 183–196

    Google Scholar 

  • Sloviter RS, Sollas AL, Dean E, Neubort S (1993) Adrenalectomy-induced granule cell degeneration in the rat hippocampal dentate gyrus: characterization of an in vivo model of controlled neuronal death. J Comp Neurol 330: 324–336

    Google Scholar 

  • Solaro CR, Lingle CJ (1992) Trypsin-sensitive, rapid inactivation of a calcium-activated potassium channel. Science 257: 1694–1698

    Google Scholar 

  • Solomon JS, Nerbonne JM (1993) Hyperpolarization-activated currents in isolated superior colliculus-projecting neurons from rat visual cortex. J Physiol (Lond) 462: 393–420

    Google Scholar 

  • Spain WJ, Schwindt PC, Crill WE (1987) Anomalous rectification in neurons from cat sensorimotor cortex in vitro. J Neurophysiol 57: 1555–1576

    Google Scholar 

  • Stabel J, Ficker E, Heinemann U (1992) Young CA1 pyramidal cells of rats, but not dentate gyrus granule cells, express a delayed inward rectifying current with properties of I Q .Neurosci Lett 135: 231–234

    Google Scholar 

  • Steinhäuser C, Tennigkeit M, Matthies H, Gündel J (1990) Properties of the fast sodium channels in pyramidal neurones isolated from the CA1 and CA3 areas of the hippocampus of postnatal rats. Pflugers Arch 415: 756–761

    Google Scholar 

  • Toselli M, Taglietti V (1990) Pharmacological characterization of voltage-dependent calcium currents in rat hippocampal neurons. Neurosci Lett 112: 70–75

    Google Scholar 

  • Zagotta WN, Hoshi T, Aldrich RW (1990) Restoration of inactivation in mutants of Shaker potassium channels by a peptide derived from ShB. Science 250: 568–571

    Google Scholar 

  • Zbicz KL, Weight FF (1985) Transient voltage and calcium-dependent outward currents in hippocampal CA3 pyramidal neurons. J Neurophysiol 53: 1038–1058

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Abteilung für Neurophysiologie, Institut für Physiologie der Charité, Humboldt Universität Berlin, Tucholskystr. 2, D-10117, Berlin, Germany

    H. Glimm, E. Ficker & U. Heinemann

Authors
  1. H. Glimm
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Ficker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. U. Heinemann
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Glimm, H., Ficker, E. & Heinemann, U. Electrophysiological properties of neurones in cultures from postnatal rat dentate gyrus. Exp Brain Res 107, 367–381 (1996). https://doi.org/10.1007/BF00230419

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00230419

Key words

Search

Navigation