Home LiteratureArticle Details
PMID: 9254663 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Slow recovery from inactivation of Na+ channels underlies the activity-dependent attenuation of dendritic action potentials in hippocampal CA1 pyramidal neurons.

Colbert CM, Magee JC, Hoffman DA, Johnston D

Abstract

Na+ action potentials propagate into the dendrites of pyramidal neurons driving an influx of Ca2+ that seems to be important for associative synaptic plasticity. During repetitive (10-50 Hz) firing, dendritic action potentials display a marked and prolonged voltage-dependent decrease in amplitude. Such a decrease is not apparent in somatic action potentials. We investigated the mechanisms of the different activity dependence of somatic and dendritic action potentials in CA1 pyramidal neurons of adult rats using whole-cell and cell-attached patch-clamp methods. There were three main findings. First, dendritic Na+ currents decreased in amplitude when repeatedly activated by brief (2 msec) depolarizations. Recovery was slow and voltage-dependent. Second, Na+ currents decreased much less in somatic than in dendritic patches. Third, although K+ currents remained constant during trains, K+ currents were necessary for dendritic action potential amplitude to decrease in whole-cell experiments. These results suggest that regional differences in Na+ and K+ channels determine the differences in the activity dependence of somatic and dendritic action potential amplitudes.

MeSH Terms
Action Potentials Animals Dendrites/physiology Electric Conductivity Electrophysiology Hippocampus/cytology,metabolism,physiology Male Potassium/physiology Pyramidal Cells/metabolism,physiology Rats Rats, Sprague-Dawley Sodium Channels/physiology
Chemicals
Sodium Channels Potassium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Colbert C M
Division of Neuroscience, Baylor College of Medicine, Houston, Texas 77030, USA.
Magee J C
Hoffman D A
Johnston D
References (27)
27 references, click to expand
  1. Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons.
    Neuron. 1989 Dec;3(6):695-704 PMID: 2561976
  2. Regenerative properties of pyramidal cell dendrites in area CA1 of the rat hippocampus.
    J Physiol. 1995 Mar 1;483 ( Pt 2):421-41 PMID: 7650611
  3. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy.
    Pflugers Arch. 1993 Jun;423(5-6):511-8 PMID: 8351200
  4. Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons.
    J Neurosci. 1997 Aug 1;17(15):5782-91 PMID: 9221776
  5. Cellular and molecular biology of voltage-gated sodium channels.
    Physiol Rev. 1992 Oct;72(4 Suppl):S15-48 PMID: 1332090
  6. Redistribution of synaptic efficacy between neocortical pyramidal neurons.
    Nature. 1996 Aug 29;382(6594):807-10 PMID: 8752273
  7. The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons.
    Nature. 1992 May 21;357(6375):244-6 PMID: 1350327
  8. Slow inactivation of Na+ current and slow cumulative spike adaptation in mouse and guinea-pig neocortical neurones in slices.
    J Physiol. 1996 May 15;493 ( Pt 1):83-97 PMID: 8735696
  9. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons.
    Nature. 1997 Jun 26;387(6636):869-75 PMID: 9202119
  10. Slow sodium channel inactivation in mammalian muscle: a possible role in regulating excitability.
    Muscle Nerve. 1988 May;11(5):502-10 PMID: 2453799
  11. Muscarinic modulation of sodium current by activation of protein kinase C in rat hippocampal neurons.
    Neuron. 1996 May;16(5):1019-26 PMID: 8630240
  12. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons.
    Science. 1997 Jan 10;275(5297):209-13 PMID: 8985013
  13. Slow inactivation of sodium channels: more than just a laboratory curiosity.
    Biophys J. 1996 Jul;71(1):5-7 PMID: 8804584
  14. Slow inactivation of the sodium conductance in squid giant axons. Pronase resistance.
    J Physiol. 1978 Oct;283:1-21 PMID: 722569
  15. Modeling the attenuation and failure of action potentials in the dendrites of hippocampal neurons.
    Biophys J. 1996 Nov;71(5):2394-403 PMID: 8913580
  16. Direct modulation of Na+ currents by protein kinase C activators in mouse neuroblastoma cells.
    J Membr Biol. 1995 Mar;144(1):59-69 PMID: 7595942
  17. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites.
    Science. 1995 Apr 14;268(5208):297-300 PMID: 7716524
  18. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites.
    Nature. 1994 Jan 6;367(6458):69-72 PMID: 8107777
  19. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs.
    Science. 1997 Jan 10;275(5297):213-5 PMID: 8985014
  20. SODIUM CONDUCTANCE SHIFT IN AN AXON INTERNALLY PERFUSED WITH A SUCROSE AND LOW-POTASSIUM SOLUTION.
    J Physiol. 1964 Aug;172:163-73 PMID: 14205014
  21. IPSPs modulate spike backpropagation and associated [Ca2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons.
    J Neurophysiol. 1996 Nov;76(5):2896-906 PMID: 8930242
  22. Functional modulation of brain sodium channels by cAMP-dependent phosphorylation.
    Neuron. 1992 Jun;8(6):1151-9 PMID: 1319185
  23. Frequency-dependent propagation of sodium action potentials in dendrites of hippocampal CA1 pyramidal neurons.
    J Neurophysiol. 1995 Oct;74(4):1395-403 PMID: 8989380
  24. Axonal action-potential initiation and Na+ channel densities in the soma and axon initial segment of subicular pyramidal neurons.
    J Neurosci. 1996 Nov 1;16(21):6676-86 PMID: 8824308
  25. Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons.
    J Physiol. 1995 Aug 15;487(1):67-90 PMID: 7473260
  26. The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons.
    J Neurosci. 1991 Jul;11(7):2270-80 PMID: 2066782
  27. Sodium and calcium currents in acutely dissociated neurons from rat suprachiasmatic nucleus.
    J Neurophysiol. 1993 Oct;70(4):1692-703 PMID: 7904302
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-09-01
Pages
6512-21
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6573147
Subset
IM
Grants
NIMH NIH HHS · MH44754 · United States
NIMH NIH HHS · MH48432 · United States
NINDS NIH HHS · NS11535 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]