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. 1996 Sep 3;93(18):9921–9925. doi: 10.1073/pnas.93.18.9921

Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo.

G Buzsáki 1, M Penttonen 1, Z Nádasdy 1, A Bragin 1
PMCID: PMC38530  PMID: 8790432

Abstract

The invasion of sodium spikes from the soma into dendrites was studied in hippocampal pyramidal cells by simultaneous extracellular and intracellular recordings in anesthetized rats and by simultaneous extracellular recordings of the somatic and dendritic potentials in freely behaving animals. During complex-spike patterns, recorded in the immobile or sleeping animal, dendritic invasion of successive spikes was substantially attenuated. Complex-spike bursts occurred in association with population discharge of CA3-CA1 pyramidal cells (sharp wave field events). Synaptic inhibition reduced the amplitude of sodium spikes in the dendrites and prevented the occurrence of calcium spikes. These findings indicate that (i) the voltage-dependent calcium influx into the dendrites is under the control of inhibitory neurons and (ii) the temporal coincidence of synaptic depolarization and activation of voltage-dependent calcium conductances by the backpropagating spikes during sharp wave bursts may be critical for synaptic plasticity in the intact hippocampus.

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Selected References

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

  1. Andersen P., Holmqvist B., Voorhoeve P. E. Entorhinal activation of dentate granule cells. Acta Physiol Scand. 1966 Apr;66(4):448–460. doi: 10.1111/j.1748-1716.1966.tb03223.x. [DOI] [PubMed] [Google Scholar]
  2. Bliss T. V., Collingridge G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993 Jan 7;361(6407):31–39. doi: 10.1038/361031a0. [DOI] [PubMed] [Google Scholar]
  3. Buhl E. H., Halasy K., Somogyi P. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature. 1994 Apr 28;368(6474):823–828. doi: 10.1038/368823a0. [DOI] [PubMed] [Google Scholar]
  4. Buzsàki G., Eidelberg E. Phase relations of hippocampal projection cells and interneurons to theta activity in the anesthetized rat. Brain Res. 1983 May 5;266(2):334–339. doi: 10.1016/0006-8993(83)90665-0. [DOI] [PubMed] [Google Scholar]
  5. Buzsáki G., Leung L. W., Vanderwolf C. H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983 Oct;287(2):139–171. doi: 10.1016/0165-0173(83)90037-1. [DOI] [PubMed] [Google Scholar]
  6. Ghosh A., Greenberg M. E. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science. 1995 Apr 14;268(5208):239–247. doi: 10.1126/science.7716515. [DOI] [PubMed] [Google Scholar]
  7. Gulyás A. I., Miles R., Hájos N., Freund T. F. Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci. 1993 Dec 1;5(12):1729–1751. doi: 10.1111/j.1460-9568.1993.tb00240.x. [DOI] [PubMed] [Google Scholar]
  8. Huguenard J. R., Hamill O. P., Prince D. A. Sodium channels in dendrites of rat cortical pyramidal neurons. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2473–2477. doi: 10.1073/pnas.86.7.2473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jaffe D. B., Johnston D., Lasser-Ross N., Lisman J. E., Miyakawa H., Ross W. N. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons. Nature. 1992 May 21;357(6375):244–246. doi: 10.1038/357244a0. [DOI] [PubMed] [Google Scholar]
  10. Llinas R., Nicholson C. Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J Neurophysiol. 1971 Jul;34(4):532–551. doi: 10.1152/jn.1971.34.4.532. [DOI] [PubMed] [Google Scholar]
  11. Magee J. C., Johnston D. Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science. 1995 Apr 14;268(5208):301–304. doi: 10.1126/science.7716525. [DOI] [PubMed] [Google Scholar]
  12. Mainen Z. F., Joerges J., Huguenard J. R., Sejnowski T. J. A model of spike initiation in neocortical pyramidal neurons. Neuron. 1995 Dec;15(6):1427–1439. doi: 10.1016/0896-6273(95)90020-9. [DOI] [PubMed] [Google Scholar]
  13. Ranck J. B., Jr Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol. 1973 Nov;41(2):461–531. doi: 10.1016/0014-4886(73)90290-2. [DOI] [PubMed] [Google Scholar]
  14. Regehr W., Kehoe J. S., Ascher P., Armstrong C. Synaptically triggered action potentials in dendrites. Neuron. 1993 Jul;11(1):145–151. doi: 10.1016/0896-6273(93)90278-y. [DOI] [PubMed] [Google Scholar]
  15. Sik A., Penttonen M., Ylinen A., Buzsáki G. Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci. 1995 Oct;15(10):6651–6665. doi: 10.1523/JNEUROSCI.15-10-06651.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Spruston N., Schiller Y., Stuart G., Sakmann B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science. 1995 Apr 14;268(5208):297–300. doi: 10.1126/science.7716524. [DOI] [PubMed] [Google Scholar]
  17. Staley K. J., Mody I. Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J Neurophysiol. 1992 Jul;68(1):197–212. doi: 10.1152/jn.1992.68.1.197. [DOI] [PubMed] [Google Scholar]
  18. Stuart G. J., Sakmann B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature. 1994 Jan 6;367(6458):69–72. doi: 10.1038/367069a0. [DOI] [PubMed] [Google Scholar]
  19. Turner R. W., Richardson T. L. Apical dendritic depolarizations and field interactions evoked by stimulation of afferent inputs to rat hippocampal CA1 pyramidal cells. Neuroscience. 1991;42(1):125–135. doi: 10.1016/0306-4522(91)90153-f. [DOI] [PubMed] [Google Scholar]
  20. Wong R. K., Prince D. A., Basbaum A. I. Intradendritic recordings from hippocampal neurons. Proc Natl Acad Sci U S A. 1979 Feb;76(2):986–990. doi: 10.1073/pnas.76.2.986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wong R. K., Prince D. A. Participation of calcium spikes during intrinsic burst firing in hippocampal neurons. Brain Res. 1978 Dec 29;159(2):385–390. doi: 10.1016/0006-8993(78)90544-9. [DOI] [PubMed] [Google Scholar]
  22. Ylinen A., Bragin A., Nádasdy Z., Jandó G., Szabó I., Sik A., Buzsáki G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci. 1995 Jan;15(1 Pt 1):30–46. doi: 10.1523/JNEUROSCI.15-01-00030.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Yuste R., Denk W. Dendritic spines as basic functional units of neuronal integration. Nature. 1995 Jun 22;375(6533):682–684. doi: 10.1038/375682a0. [DOI] [PubMed] [Google Scholar]

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