Home LiteratureArticle Details
PMID: 20194128 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Functional interplay between NMDA receptors, SK channels and voltage-gated Ca2+ channels regulates synaptic excitability in the medial prefrontal cortex.

The Journal of physiology ·Vol. 588 ·No. Pt 8 ·2010-04-15 ·Pages 1281-92

Faber ES

Abstract

Synaptic activity in the medial prefrontal cortex (mPFC) is fundamental for higher cognitive functions such as working memory. The present study shows that small conductance (SK) calcium-activated potassium channels attenuate excitatory synaptic transmission at layer 2/3 and layer 5 inputs to layer 5 pyramidal neurons in the mPFC. SK channels are located postsynaptically at synapses where they are activated during synaptic transmission by calcium influx through NMDA receptors, L-type calcium channels, R-type calcium channels and by calcium release from IP(3)-sensitive stores. Removal of the SK channel-mediated shunt of synaptic transmission reveals significant NMDA receptor-mediated activation during basal synaptic transmission, which is greater at layer 5 inputs (approximately 30%) than at layer 2/3 inputs (approximately 20%). These findings show that interactions between NMDA receptors, SK channels and voltage-gated calcium channels play a critical role in regulating excitatory synaptic transmission in layer 5 pyramidal neurons in the mPFC.

MeSH Terms
Animals Calcium/metabolism Calcium Channels, L-Type/physiology Calcium Channels, R-Type/physiology Cell Communication Female Male Models, Animal Potassium Channels, Voltage-Gated/physiology Prefrontal Cortex/physiology Pyramidal Cells/cytology,physiology Rats Rats, Wistar Receptors, N-Methyl-D-Aspartate/physiology Small-Conductance Calcium-Activated Potassium Channels/physiology Synapses/physiology Synaptic Transmission/physiology
Chemicals
Calcium Channels, L-Type Calcium Channels, R-Type Potassium Channels, Voltage-Gated Receptors, N-Methyl-D-Aspartate Small-Conductance Calcium-Activated Potassium Channels Calcium
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Faber E S L
Queensland Brain Institute, The University of Queensland, Brisbane, QLD 4072, Australia. [email protected]
References (40)
40 references, click to expand
  1. Bicuculline methiodide potentiates NMDA-dependent burst firing in rat dopamine neurons by blocking apamin-sensitive Ca2+-activated K+ currents.
    Neurosci Lett. 1997 Aug 1;231(1):13-6 PMID: 9280156
  2. Small-conductance Ca2+-dependent K+ channels are the target of spike-induced Ca2+ release in a feedback regulation of pyramidal cell excitability.
    J Neurophysiol. 2004 May;91(5):2322-9 PMID: 14695351
  3. Synaptic reverberation underlying mnemonic persistent activity.
    Trends Neurosci. 2001 Aug;24(8):455-63 PMID: 11476885
  4. Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory.
    J Neurophysiol. 1973 Jan;36(1):61-78 PMID: 4196203
  5. SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines.
    Nat Neurosci. 2005 May;8(5):642-9 PMID: 15852011
  6. Learning rules for spike timing-dependent plasticity depend on dendritic synapse location.
    J Neurosci. 2006 Oct 11;26(41):10420-9 PMID: 17035526
  7. Intracellular calcium store filling by an L-type calcium current in the basolateral amygdala at subthreshold membrane potentials.
    J Physiol. 2005 Jan 15;562(Pt 2):439-53 PMID: 15550460
  8. The "psychic" neuron of the cerebral cortex.
    Ann N Y Acad Sci. 1999 Apr 30;868:13-26 PMID: 10414278
  9. MGluR-mediated calcium waves that invade the soma regulate firing in layer V medial prefrontal cortical pyramidal neurons.
    Cereb Cortex. 2008 Feb;18(2):407-23 PMID: 17573372
  10. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study.
    J Anat. 1959 Oct;93:420-33 PMID: 13829103
  11. Differential distribution of three Ca(2+)-activated K(+) channel subunits, SK1, SK2, and SK3, in the adult rat central nervous system.
    Mol Cell Neurosci. 2000 May;15(5):476-93 PMID: 10833304
  12. Differential paired pulse depression of non-NMDA and NMDA currents in pyramidal cells of the rat frontal cortex.
    J Neurosci. 1995 Dec;15(12):8268-80 PMID: 8613760
  13. Neurocomputational models of working memory.
    Nat Neurosci. 2000 Nov;3 Suppl:1184-91 PMID: 11127836
  14. Increased threshold for spike-timing-dependent plasticity is caused by unreliable calcium signaling in mice lacking fragile X gene FMR1.
    Neuron. 2007 May 24;54(4):627-38 PMID: 17521574
  15. Analysis of calcium channels in single spines using optical fluctuation analysis.
    Nature. 2000 Nov 30;408(6812):589-93 PMID: 11117746
  16. L-type calcium channels: highs and new lows.
    Circ Res. 2002 May 17;90(9):933-5 PMID: 12016257
  17. Three-dimensional analysis of dendritic spines. I. Quantitative observations related to dendritic spine and synaptic morphology in cerebral and cerebellar cortices.
    Anat Embryol (Berl). 1983;167(2):289-310 PMID: 6614508
  18. Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines.
    Neuron. 2007 Jan 18;53(2):249-60 PMID: 17224406
  19. Dihydropyridine-sensitive, voltage-gated Ca2+ channels contribute to the resting intracellular Ca2+ concentration of hippocampal CA1 pyramidal neurons.
    J Neurophysiol. 1996 Nov;76(5):3460-70 PMID: 8930286
  20. A specialized NMDA receptor function in layer 5 recurrent microcircuitry of the adult rat prefrontal cortex.
    Proc Natl Acad Sci U S A. 2008 Oct 28;105(43):16791-6 PMID: 18922773
  21. Nomenclature of voltage-gated calcium channels.
    Neuron. 2000 Mar;25(3):533-5 PMID: 10774722
  22. A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons.
    Neuron. 2006 Jul 20;51(2):227-38 PMID: 16846857
  23. On the electrical function of dendritic spines.
    Trends Neurosci. 2004 Feb;27(2):77-83 PMID: 15102486
  24. SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala.
    Nat Neurosci. 2005 May;8(5):635-41 PMID: 15852010
  25. Blockade of IP3-mediated SK channel signaling in the rat medial prefrontal cortex improves spatial working memory.
    Learn Mem. 2008 Feb 19;15(3):93-6 PMID: 18285467
  26. Catecholamine and second messenger influences on prefrontal cortical networks of "representational knowledge": a rational bridge between genetics and the symptoms of mental illness.
    Cereb Cortex. 2007 Sep;17 Suppl 1:i6-15 PMID: 17434919
  27. SK2 channel plasticity contributes to LTP at Schaffer collateral-CA1 synapses.
    Nat Neurosci. 2008 Feb;11(2):170-7 PMID: 18204442
  28. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones.
    Nature. 1984 May 17-23;309(5965):261-3 PMID: 6325946
  29. Expression of N-methyl-D-aspartate receptor subunit mRNAs in the human brain: hippocampus and cortex.
    J Comp Neurol. 1998 Jan 5;390(1):75-90 PMID: 9456177
  30. Calcium activates two types of potassium channels in rat hippocampal neurons in culture.
    J Neurosci. 1991 Jan;11(1):23-30 PMID: 1986065
  31. Heterogeneity of phasic cholinergic signaling in neocortical neurons.
    J Neurophysiol. 2007 Mar;97(3):2215-29 PMID: 17122323
  32. Multiple channel types contribute to the low-voltage-activated calcium current in hippocampal CA3 pyramidal neurons.
    J Neurosci. 1996 Sep 15;16(18):5567-82 PMID: 8795613
  33. Regional expression and cellular localization of the alpha1 and beta subunit of high voltage-activated calcium channels in rat brain.
    J Neurosci. 1997 Feb 15;17(4):1339-49 PMID: 9006977
  34. Functions of SK channels in central neurons.
    Clin Exp Pharmacol Physiol. 2007 Oct;34(10):1077-83 PMID: 17714097
  35. Reporting ethical matters in the Journal of Physiology: standards and advice.
    J Physiol. 2009 Feb 15;587(Pt 4):713-9 PMID: 19218620
  36. Cellular basis of working memory.
    Neuron. 1995 Mar;14(3):477-85 PMID: 7695894
  37. Small-conductance, calcium-activated potassium channels from mammalian brain.
    Science. 1996 Sep 20;273(5282):1709-14 PMID: 8781233
  38. The contribution of intracellular calcium stores to mEPSCs recorded in layer II neurones of rat barrel cortex.
    J Physiol. 2002 Dec 1;545(2):521-35 PMID: 12456831
  39. Regional differences in distribution and functional expression of small-conductance Ca2+-activated K+ channels in rat brain.
    J Neurosci. 2002 Nov 15;22(22):9698-707 PMID: 12427825
  40. Modulation of SK channel trafficking by beta adrenoceptors enhances excitatory synaptic transmission and plasticity in the amygdala.
    J Neurosci. 2008 Oct 22;28(43):10803-13 PMID: 18945888
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
1469-7793
Published
2010-04-15
Epub
2010-00-01
Pages
1281-92
Language
English
Region
England
NLM ID
0266262
PMCID
PMC2872733
Subset
IM
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]