Home LiteratureArticle Details
PMID: 21187403 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Arc-dependent synapse-specific homeostatic plasticity.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 108 ·No. 2 ·2011-01-11 ·Pages 816-21

Béïque JC, Na Y, Kuhl D, Worley PF, Huganir RL

Abstract

Both theoretical and experimental research has indicated that the synaptic strength between neurons in a network needs to be properly fine-tuned and controlled by homeostatic mechanisms to ensure proper network function. One such mechanism that has been extensively characterized is synaptic homeostatic plasticity or global synaptic scaling. This mechanism refers to the bidirectional ability of all synapses impinging on a neuron to actively compensate for changes in the neuron's overall excitability. Here, using a combination of electrophysiological, two-photon glutamate uncaging and imaging methods, we show that mature individual synapses, independent of neighboring synapses, have the ability to autonomously sense their level of activity and actively compensate for it in a homeostatic-like fashion. This synapse-specific homeostatic plasticity, similar to global synaptic plasticity, requires the immediate early gene Arc. Together, our results document an extra level of regulation of synaptic function that bears important computational consequences on information storage in the brain.

MeSH Terms
Animals Homeostasis/physiology Mice Mice, Knockout Models, Biological Models, Neurological Neuronal Plasticity/physiology Neurons/metabolism Patch-Clamp Techniques Receptors, AMPA/metabolism Synapses/metabolism,physiology Synaptic Transmission
Chemicals
Receptors, AMPA glutamate receptor ionotropic, AMPA 2
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Béïque Jean-Claude
The Solomon Snyder Department of Neuroscience, Johns Hopkins University, USA.
Na Youn
Kuhl Dietmar
Worley Paul F
Huganir Richard L
References (44)
44 references, click to expand
  1. Synapse-specific regulation of AMPA receptor subunit composition by activity.
    J Neurosci. 2005 Jul 6;25(27):6379-88 PMID: 16000628
  2. Metaplasticity at single glutamatergic synapses.
    Neuron. 2010 Jun 24;66(6):859-70 PMID: 20620872
  3. Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons.
    J Physiol. 1995 Jan 15;482 ( Pt 2):325-52 PMID: 7536248
  4. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis.
    Cell. 2006 May 19;125(4):785-99 PMID: 16713568
  5. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses.
    Neuron. 2004 Dec 2;44(5):749-57 PMID: 15572107
  6. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons.
    Nat Neurosci. 2001 Nov;4(11):1086-92 PMID: 11687814
  7. Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites.
    Neuron. 1998 Oct;21(4):741-51 PMID: 9808461
  8. Double dissociation between long-term depression and dendritic spine morphology in cerebellar Purkinje cells.
    Nat Neurosci. 2007 May;10(5):546-8 PMID: 17435753
  9. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation.
    Nat Neurosci. 2006 May;9(5):602-4 PMID: 16582904
  10. Synapse-specific regulation of AMPA receptor function by PSD-95.
    Proc Natl Acad Sci U S A. 2006 Dec 19;103(51):19535-40 PMID: 17148601
  11. Developmental presence and disappearance of postsynaptically silent synapses on dendritic spines of rat layer 2/3 pyramidal neurons.
    J Physiol. 2008 Mar 15;586(6):1519-27 PMID: 18202095
  12. Long-term depression in hippocampal interneurons: joint requirement for pre- and postsynaptic events.
    Science. 1999 Aug 27;285(5432):1411-4 PMID: 10464102
  13. Synaptic plasticity: taming the beast.
    Nat Neurosci. 2000 Nov;3 Suppl:1178-83 PMID: 11127835
  14. The self-tuning neuron: synaptic scaling of excitatory synapses.
    Cell. 2008 Oct 31;135(3):422-35 PMID: 18984155
  15. Rapid synaptic scaling induced by changes in postsynaptic firing.
    Neuron. 2008 Mar 27;57(6):819-26 PMID: 18367083
  16. Adaptation to synaptic inactivity in hippocampal neurons.
    Neuron. 2005 Sep 1;47(5):725-37 PMID: 16129401
  17. Pathway-specific trafficking of native AMPARs by in vivo experience.
    Neuron. 2006 Mar 2;49(5):663-70 PMID: 16504942
  18. Synaptic scaling mediated by glial TNF-alpha.
    Nature. 2006 Apr 20;440(7087):1054-9 PMID: 16547515
  19. Impaired regulation of synaptic strength in hippocampal neurons from GluR1-deficient mice.
    J Physiol. 2003 Oct 1;552(Pt 1):35-45 PMID: 12878757
  20. Homeostatic plasticity studied using in vivo hippocampal activity-blockade: synaptic scaling, intrinsic plasticity and age-dependence.
    PLoS One. 2007 Aug 08;2(8):e700 PMID: 17684547
  21. Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins.
    Neuron. 2008 Jun 12;58(5):749-62 PMID: 18549786
  22. Synapse-specific adaptations to inactivity in hippocampal circuits achieve homeostatic gain control while dampening network reverberation.
    Neuron. 2008 Jun 26;58(6):925-37 PMID: 18579082
  23. Homeostatic regulation of AMPA receptor expression at single hippocampal synapses.
    Proc Natl Acad Sci U S A. 2008 Jan 15;105(2):775-80 PMID: 18174334
  24. LTP and adaptation to inactivity: overlapping mechanisms and implications for metaplasticity.
    Neuropharmacology. 2007 Jan;52(1):156-75 PMID: 16949624
  25. Long-term potentiation in the hippocampal CA1 region does not require insertion and activation of GluR2-lacking AMPA receptors.
    J Neurophysiol. 2007 Oct;98(4):2488-92 PMID: 17652419
  26. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity.
    Neuron. 2007 Jun 21;54(6):859-71 PMID: 17582328
  27. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories.
    Neuron. 2006 Nov 9;52(3):437-44 PMID: 17088210
  28. Anatomical and physiological plasticity of dendritic spines.
    Annu Rev Neurosci. 2007;30:79-97 PMID: 17280523
  29. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach.
    Neuron. 2009 Apr 30;62(2):254-68 PMID: 19409270
  30. Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation.
    J Neurosci. 2007 Apr 25;27(17):4598-602 PMID: 17460072
  31. Structural basis of long-term potentiation in single dendritic spines.
    Nature. 2004 Jun 17;429(6993):761-6 PMID: 15190253
  32. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses.
    Nat Neurosci. 1999 Jul;2(7):618-24 PMID: 10409387
  33. Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors.
    Neuron. 2006 Nov 9;52(3):475-84 PMID: 17088213
  34. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons.
    J Neurosci. 1996 Mar 15;16(6):1982-9 PMID: 8604042
  35. The cell biology of synaptic plasticity: AMPA receptor trafficking.
    Annu Rev Cell Dev Biol. 2007;23:613-43 PMID: 17506699
  36. Activity-dependent scaling of quantal amplitude in neocortical neurons.
    Nature. 1998 Feb 26;391(6670):892-6 PMID: 9495341
  37. Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity.
    Neuron. 2007 May 3;54(3):447-60 PMID: 17481397
  38. AMPA receptor subunits get their share of the pie.
    Neuron. 2009 Apr 30;62(2):165-8 PMID: 19409261
  39. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons.
    Nature. 2002 Nov 28;420(6914):414-8 PMID: 12459783
  40. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking.
    Neuron. 2006 Nov 9;52(3):445-59 PMID: 17088211
  41. Stabilization of Ca2+-permeable AMPA receptors at perisynaptic sites by GluR1-S845 phosphorylation.
    Proc Natl Acad Sci U S A. 2009 Nov 24;106(47):20033-8 PMID: 19892736
  42. Activity-dependent modulation of synaptic AMPA receptor accumulation.
    Neuron. 1998 Nov;21(5):1067-78 PMID: 9856462
  43. Postsynaptic expression of homeostatic plasticity at neocortical synapses.
    J Neurosci. 2005 Mar 16;25(11):2895-905 PMID: 15772349
  44. Homeostatic plasticity in the developing nervous system.
    Nat Rev Neurosci. 2004 Feb;5(2):97-107 PMID: 14735113
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
DOI
10.1073/pnas.1017914108
Published
2011-01-11
Epub
2010-00-27
Pages
816-21
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3021034
Subset
IM
Grants
Howard Hughes Medical Institute · United States
External Links
PubMed source DOI: 10.1073/pnas.1017914108 PMC Full Text View journal details
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]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2