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Experimental Brain Research

, Volume 79, Issue 3, pp 633–641 | Cite as

A decrease in firing threshold observed after induction of the EPSP-spike (E-S) component of long-term potentiation in rat hippocampal slices

  • L. E. Chavez-Noriega
  • J. V. Halliwell
  • T. V. P. Bliss
Article

Summary

Two components of long-term potentiation (LTP) are distinguished with extracellular recording electrodes: a synaptic and an EPSP-Spike (E-S) component. The latter consists of the enhancement produced in the population spike amplitude in excess of that predicted by EPSP potentiation alone. The experiments carried out in this study were designed to investigate intracellular correlates of E-S potentiation and to examine the hypothesis that an increased postsynaptic excitability underlies E-S potentiation. CA1 pyramidal neurons were synaptically activated from stratum radiatum. LTP, defined as a stable increase in the probability of firing to afferent stimulation, was found to be related to a decrease in the intracellular PSP peak amplitude and slope required to fire the cells at a probability of 0.5. These changes were accompanied by a decrease in threshold to direct activation. No significant changes in input resistance or resting potential were recorded. These excitability changes were only observed in cells displaying LTP; they were not related to the potentiation of the synaptic component (PSP amplitude). Our results support the hypothesis that different mechanisms underlie the two components of LTP, and that a reduction in threshold for neuronal discharge accompanies tetanus-induced E-S potentiation. It is suggested that an increase in the ratio of synaptically evoked excitation/inhibition and a reduction in tonic synaptic inhibition through GA-BAA channels contribute to E-S potentiation.

Key words

Long-term potentiation Hippocampus CA1 Inhibition Rat 

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References

  1. Abraham WC, Bliss TVP, Goddard GV (1985) Heterosynaptic changes accompany long-term but not short-term potentiation of the perforant path in the anaesthetized rat. J Physiol (Lond) 363:335–349Google Scholar
  2. Abraham WC, Gustafsson B, Wigstrom H (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. J Physiol (Lond) 394:367–380Google Scholar
  3. Alger BE, Nicoll RA (1980) Spontaneous inhibitory post-synaptic potentials in hippocampus: mechanism for tonic inhibition. Brain Res 200:195–200Google Scholar
  4. Andersen P, Avoli M, Hvalby O (1984) Evidence for both pre-and postsynaptic mechanisms during long-term potentiation in hippocampal slices. Exp Brain Res Suppl 9:315–324Google Scholar
  5. Andersen P, Eccles JC, Loyning Y (1964) Pathway of postsynaptic inhibition in the hippocampus. J Neurophysiol 27:608–619Google Scholar
  6. Andersen P, Hvalby O, Reymann K (1988) Postsynaptic mechanisms contribute to the synaptic potentiation induced by phorbol esters in rat hippocampal pyramidal cells in vitro. J Physiol (Lond) 398:24PGoogle Scholar
  7. Andersen P, Sundberg SH, Sveen O, Swann JW, Wigstrom H (1980) Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea pigs. J Physiol (Lond) 302:463–482Google Scholar
  8. Andersen P, Storm J, Wheal HV (1987) Thresholds of action potentials evoked by synapses on the dendrites of pyramidal cells in the rat hippocampus in vitro. J Physiol (Lond) 383:509–526Google Scholar
  9. Ashwood TJ, Collingridge GL, Herron CE, Wheal HV (1987) Voltage-clamp analysis of somatic gamma-aminobutyric acid responses in adult rat hippocampal CA1 neurones in vitro. J Physiol (Lond) 384:27–37Google Scholar
  10. Barrionuevo G, Brown TH (1983) Associative long-term potentiation in hippocampal slices. Proc Natl Acad Sci USA 80:7347–7351Google Scholar
  11. Barrionuevo G, Kelso S, Johnston D, Brown TH (1986) Conductance mechanism responsible for long-term potentiation in monosynaptic and isolated excitatory synaptic inputs to hippocampus. J Neurophysiol 55:540–550Google Scholar
  12. Blackstad TW, Flood PR (1963) Ultrastructure of hippocampal axo-somatic synapses. Nature (Lond) 198:542–543Google Scholar
  13. Bliss TVP, Chavez-Noriega LE (1988) Gabaergic, but not cholinergic, mechanisms contribute to the EPSP-spike (E-S) component of long-term potentiation in the rat hippocampal slice. J Physiol (Lond) 399:66PGoogle Scholar
  14. Bliss TVP, Chavez-Noriega LE, Halliwell JV (1987a) Longterm potentiation is associated with an increase in the excitability of pyramidal cells in area CA1 of the rat hippocampal slice. J Physiol (Lond) 390:260PGoogle Scholar
  15. Bliss TVP, Douglas RM, Errington ML, Lynch MA (1986) Correlation between long-term potentiation and release of endogenous amino acids from dentate gyrus of anaesthetized rats. J Physiol (Lond) 377:391–408Google Scholar
  16. Bliss RVP, Errington ML, Lynch MA (1987b) Calcium-induced long-term potentiation in the dentate gyrus is accompanied by a sustained increase in glutamate release. In: Hicks TP, Lodge D (eds) Excitatory amino acid transmission. Alan R Liss, New York, pp 337–340Google Scholar
  17. Bliss TVP, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:357–374Google Scholar
  18. Bliss TVP, Gardner-Medwin AR, Lomo T (1973) Synaptic plasticity in the hippocampal formation. In: Ansell GB, Bradley PB (eds) Macromolecules and behaviour. Macmillan, London, pp 193–203Google Scholar
  19. Bliss TVP, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331–356Google Scholar
  20. Bliss TVP, Lynch MA (1988) Long-term potentiation of synaptic transmission in the hippocampus: properties and mechanisms. In: Landfield PW, Deadwyler SA (eds) Long-term potentiation: from biophysics to behavior. Alan R Liss, New York, pp 3–72Google Scholar
  21. Catterall WA (1981) Localization of sodium channels in cultured neural cells. J Neurosci 1:777–783Google Scholar
  22. Chavez-Noriega LE, Bliss TVP, Halliwell JV (1987) Long-term potentiation in area CA1 of the hippocampus is not associated with changes in calcium-dependent afterhyperpolarization. Neurosci Lett Suppl 29:S97Google Scholar
  23. Chavez-Noriega LE, Bliss TVP, Halliwell JV (1989) The EPSP-spike (E-S) component of long-term potentiation in the rat hippocampal slice is modulated by GABAergic but not cholinergic mechanisms. Neurosci Lett 104:58–64Google Scholar
  24. Collingridge GL, Kehl SJ, McLennan H (1983) Excitatory amino acids in synaptic transmission in the Schaffer collateralcommissural pathway of the rat hippocampus. J Physiol (Lond) 334:33–46Google Scholar
  25. Dingledine R, Gjerstad L (1980) Reduced inhibition during epileptiform activity in the in vitro hippocampal slice. J Physiol (Lond) 305:297–313Google Scholar
  26. Douglas RM, Goddard GV (1975) Long-term potentiation of the perforant path-granule cell synapse in the rat hippocampus. Brain Res 86:205–215Google Scholar
  27. Eccles JC, Nicoll RA, Oshima T, Rubia FJ (1977) The anionic permeability of the inhibitory postsynaptic membrane of hippocampal pyramidal cells. Proc R Soc Lond B 198:345–361Google Scholar
  28. Haas HL, Jefferys JGR (1984) Low-calcium field burst discharges of CA1 pyramidal neurones in rat hippocampal slices. J Physiol (Lond) 354:185–201Google Scholar
  29. Hamill OP, Bormann J, Sakmann B (1983) Activation of multiple-conductance state chloride channels in spinal neurones by glycine and GABA. Nature (Lond) 305:805–808Google Scholar
  30. Hotson JR, Prince DA (1980) A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J Neurophysiol 43:409–419Google Scholar
  31. Hu G-Y, Hvalby O, Walaas SI, Albert KA, Skjeflo P, Andersen P, Greengard P (1987) Protein kinase C injection into hippocampal pyramidal cells elicits features of long-term potentiation. Nature (Lond) 328:426–429Google Scholar
  32. Huguenard JR, Alger BE (1986) Whole-cell voltage-clamp study of the fading of GABA-activated currents in acutely dissociated hippocampal neurons. J Neurophysiol 56:1–18Google Scholar
  33. Hvalby O, Lacaille JC, Hu G-Y, Andersen P (1987) Postsynaptic long-term potentiation follows coupling of dendritic glutamate application and synaptic activation. Experientia 43:599–601Google Scholar
  34. Kandel ER, Spencer WA, Brinley FJ (1961) Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. J Neurophysiol 24:225–241Google Scholar
  35. Katz B (1966) Nerve, muscle and synapse. McGraw-Hill, LondonGoogle Scholar
  36. Kelso SR, Ganong AH, Brown TH (1986) Hebbian synapses in hippocampus. Proc Natl Acad Sci USA 83:5326–5330Google Scholar
  37. Lancaster B, Adams PR (1986) A calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. J Neurophysiol 55:1268–1282Google Scholar
  38. Malenka RC, Madison DV, Nicoll RA (1986) Potentiation of synaptic transmission in the hippocampus by phorbol esters. Nature (Lond) 321:175–177Google Scholar
  39. Malinow R, Madison DV, Tsien RW (1988) Persistent protein kinase activity underlying long-term potentiation. Nature (Lond) 335:820–824Google Scholar
  40. McNaughton BL, Barnes CA (1977) Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathways in the rat. J Comp Neurol 175:439–454Google Scholar
  41. McNaughton BL, Douglas RM, Goddard GV (1978) Synaptic enhancement in fascia dentata: cooperativity among coactive afferents. Brain Res 157:277–293Google Scholar
  42. Melchers BPC, Pennartz CMA, Lopes da Silva FH (1987) Differential effects of elevated extracellular calcium concentrations on field potentials in dentate gyrus and CA1 of the rat hippocampal slice preparation. Neurosci Lett 77:37–42Google Scholar
  43. Moore JW, Westerfield M (1983) Action potential propagation and threshold parameters in inhomogeneous regions of squid axons. J Physiol (Lond) 336:285–300Google Scholar
  44. Pinter MJ, Curtis RL, Hosko MJ (1983) Voltage threshold and excitability among variously sized cat hindlimb motoneurons. J Neurophysiol 50:644–657Google Scholar
  45. Reymann KG, Matthies HK, Frey U, Vorobyev VS, Matthies H (1986) Calcium-induced long-term potentiation in the hippocampal slice: characterization of the time course and conditions. Brain Res Bull 17:291–296Google Scholar
  46. Ribak ChE, Vaughn JE, Saito K (1978) Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res 140:315–332Google Scholar
  47. Richter DW, Schlue WR, Mauritz KH, Nacimiento AC (1974) Comparison of membrane properties of the cell body and the initial part of the axon of phasic motoneurones in the spinal chord of the cat. Exp Brain Res 21:193–206Google Scholar
  48. Schwartzkroin PA (1977) Further characteristics of hippocampal CA1 cells in vitro. Brain Res 128:53–68Google Scholar
  49. Sigel E, Baur R (1988) Activation of protein kinase C differentially modulates neuronal Na+, Ca2+, and gamma-aminobutyrate type A channels. Proc Natl Acad Sci USA 85:6192–6196Google Scholar
  50. Somogyi P, Nunzi MG, Gorio A, Smith AD (1983a) A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res 259:137–142Google Scholar
  51. Somogyi P, Smith AD, Nunzi MG, Gorio A, Takagi H, Wu JY (1983b) Glutamate decarboxylase immunoreactivity in the hippocampus of the cat: distribution of immunoreactivity in the hippocampus of the cat and distribution of immunoreactive synaptic terminals with special reference to the axon initial segment of pyramidal neurons. J Neurosci 3:1450–1468Google Scholar
  52. Stelzer A, Slater NT, Bruggencate GT (1987) Activation of NMDA receptors blocks GABAergic inhibition in an in vitro model of epilepsy. Nature (Lond) 326:698–701Google Scholar
  53. Storm-Mathisen J, Fonnum F (1971) Quantitative histochemistry of glutamate decarboxylase in the rat hippocampal region. J Neurochem 18:1105–1111Google Scholar
  54. Taube JS, Schwartzkroin PA (1988a) Mechanisms of long-term potentiation: EPSP/spike dissociation, intradendritic recordings and glutamate sensitivity. J Neurosci 8:1632–1644Google Scholar
  55. Taube JS, Schwartzkroin PA (1988b) Mechanisms of long-term potentiation: a current-source density analysis. J Neurosci 8:1645–1655Google Scholar
  56. Taylor CP, Dudek FE (1984) Excitation of hippocampal pyramidal cells by an electrical field effect. J Neurophysiol 52:126–142Google Scholar
  57. Teyler TJ, DiScenna P (1987) Long-term potentiation. Ann Rev Neurosci 10:131–161Google Scholar
  58. Turner RW, Baimbridge KG, Miller JJ (1982) Calcium-induced long-term potentiation in the hippocampus. Neuroscience 7:1411–1416Google Scholar
  59. Wigstrom H, Gustafsson B (1983) Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature (Lond) 301:603–604Google Scholar
  60. Wilson RC, Levy WB, Steward O (1981) Changes in translation of synaptic excitation to dentate granule cell discharge accompanying long-term potentiation. II. An evaluation of mechanisms utilizing dentate gyrus dually innervated by surviving ipsilateral and sprouted crossed temporodentate inputs. J Neurophysiol 46:339–355Google Scholar
  61. Wong RKS, Prince DA (1981) Afterpotential generation in hippocampal pyramidal cells. J Neurophysiol 45:86–97Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • L. E. Chavez-Noriega
    • 1
  • J. V. Halliwell
    • 2
  • T. V. P. Bliss
    • 1
  1. 1.Division of Neurophysiology and NeuropharmacologyNational Institute for Medical ResearchLondonUK
  2. 2.Department of PharmacologyUniversity College LondonLondonUK

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