Home LiteratureArticle Details
PMID: 18549780 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Tumor necrosis factor-alpha mediates one component of competitive, experience-dependent plasticity in developing visual cortex.

Neuron ·Vol. 58 ·No. 5 ·2008-06-12 ·Pages 673-80

Kaneko M, Stellwagen D, Malenka RC, Stryker MP

Abstract

Rapid, experience-dependent plasticity in developing visual cortex is thought to be competitive. After monocular visual deprivation, the reduction in response of binocular neurons to one eye is matched by a corresponding increase to the other. Chronic optical imaging in mice deficient in TNFalpha reveals the normal initial loss of deprived-eye responses, but the subsequent increase in response to the open eye is absent. This mutation also blocks homeostatic synaptic scaling of mEPSCs in visual cortex in vitro, without affecting LTP. In monocular cortex, thought not to be subject to competition, responses in TNFalpha mutants are as reduced as in the binocular zone. Pharmacological inhibition of endogenous TNFalpha in wild-type mice phenocopies the knockout. These findings suggest that experience-dependent competition in developing visual cortex is the outcome of two distinct, noncompetitive processes, a loss of deprived-eye responses followed by an apparently homeostatic increase in responses dependent on TNFalpha signaling.

MeSH Terms
Analysis of Variance Animals Animals, Newborn Dominance, Ocular/physiology Excitatory Amino Acid Antagonists/pharmacology Long-Term Potentiation/drug effects,genetics,radiation effects Mice Mice, Knockout Neuronal Plasticity/drug effects,genetics,radiation effects Organ Culture Techniques Patch-Clamp Techniques/methods Sensory Deprivation/physiology Tumor Necrosis Factor-alpha/deficiency,physiology Visual Cortex/cytology,growth & development Visual Pathways/physiology
Chemicals
Excitatory Amino Acid Antagonists Tumor Necrosis Factor-alpha
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kaneko Megumi
Department of Physiology and W.M. Keck Foundation Center for Integrative Neuroscience, University of California, San Francisco, San Francisco, CA 94143-0444, USA.
Stellwagen David
Malenka Robert C
Stryker Michael P
References (46)
46 references, click to expand
  1. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation.
    Vision Res. 1994 Mar;34(6):709-20 PMID: 8160387
  2. Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex.
    J Neurosci. 2007 Jun 20;27(25):6692-700 PMID: 17581956
  3. Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory.
    Nature. 2001 May 17;411(6835):309-13 PMID: 11357133
  4. New paradigm for optical imaging: temporally encoded maps of intrinsic signal.
    Neuron. 2003 May 22;38(4):529-45 PMID: 12765606
  5. Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors.
    Neuron. 2006 Nov 9;52(3):475-84 PMID: 17088213
  6. Hebbian synapses in visual cortex.
    J Neurosci. 1994 Mar;14(3 Pt 2):1634-45 PMID: 8126560
  7. Synaptic activity and the construction of cortical circuits.
    Science. 1996 Nov 15;274(5290):1133-8 PMID: 8895456
  8. Progressive changes in kitten striate cortex during monocular vision.
    J Neurophysiol. 1975 Jan;38(1):26-32 PMID: 162944
  9. BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses.
    Neuron. 1998 Sep;21(3):521-30 PMID: 9768839
  10. Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity.
    Neuron. 2007 Jun 21;54(6):961-72 PMID: 17582335
  11. Rapid ocular dominance plasticity requires cortical but not geniculate protein synthesis.
    Neuron. 2002 Apr 25;34(3):425-36 PMID: 11988173
  12. Autophosphorylation of alphaCaMKII is required for ocular dominance plasticity.
    Neuron. 2002 Oct 24;36(3):483-91 PMID: 12408850
  13. Homeostatic plasticity in the developing nervous system.
    Nat Rev Neurosci. 2004 Feb;5(2):97-107 PMID: 14735113
  14. Deprivation-induced synaptic depression by distinct mechanisms in different layers of mouse visual cortex.
    Proc Natl Acad Sci U S A. 2007 Jan 23;104(4):1383-8 PMID: 17227847
  15. Permissive proteolytic activity for visual cortical plasticity.
    Proc Natl Acad Sci U S A. 2002 May 28;99(11):7717-21 PMID: 12032349
  16. Requirement for the RIIbeta isoform of PKA, but not calcium-stimulated adenylyl cyclase, in visual cortical plasticity.
    J Neurosci. 2004 Oct 13;24(41):9049-58 PMID: 15483123
  17. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex.
    Cell. 1999 Sep 17;98(6):739-55 PMID: 10499792
  18. "Inflammatory" cytokines: neuromodulators in normal brain?
    J Neurochem. 2000 Feb;74(2):457-71 PMID: 10646496
  19. Local GABA circuit control of experience-dependent plasticity in developing visual cortex.
    Science. 1998 Nov 20;282(5393):1504-8 PMID: 9822384
  20. Ocular dominance column development: analysis and simulation.
    Science. 1989 Aug 11;245(4918):605-15 PMID: 2762813
  21. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex.
    J Neurosci. 1982 Jan;2(1):32-48 PMID: 7054394
  22. Synaptic scaling mediated by glial TNF-alpha.
    Nature. 2006 Apr 20;440(7087):1054-9 PMID: 16547515
  23. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse.
    J Neurosci. 1996 May 15;16(10):3274-86 PMID: 8627365
  24. Chronic recordings from single sites of kitten striate cortex during experience-dependent modifications of receptive-field properties.
    J Neurophysiol. 1989 Jul;62(1):185-97 PMID: 2754471
  25. Optical imaging of the intrinsic signal as a measure of cortical plasticity in the mouse.
    Vis Neurosci. 2005 Sep-Oct;22(5):685-91 PMID: 16332279
  26. Reduced ocular dominance plasticity and long-term potentiation in the developing visual cortex of protein kinase A RII alpha mutant mice.
    Eur J Neurosci. 2004 Aug;20(3):837-42 PMID: 15255994
  27. Deficient plasticity in the primary visual cortex of alpha-calcium/calmodulin-dependent protein kinase II mutant mice.
    Neuron. 1996 Sep;17(3):491-9 PMID: 8816712
  28. Critical period plasticity in local cortical circuits.
    Nat Rev Neurosci. 2005 Nov;6(11):877-88 PMID: 16261181
  29. How monocular deprivation shifts ocular dominance in visual cortex of young mice.
    Neuron. 2004 Dec 16;44(6):917-23 PMID: 15603735
  30. Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex.
    J Neurosci. 1999 Nov 15;19(22):RC40 PMID: 10559430
  31. PirB restricts ocular-dominance plasticity in visual cortex.
    Science. 2006 Sep 22;313(5794):1795-800 PMID: 16917027
  32. Maintaining the stability of neural function: a homeostatic hypothesis.
    Annu Rev Physiol. 2001;63:847-69 PMID: 11181978
  33. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.
    J Physiol. 1962 Jan;160:106-54 PMID: 14449617
  34. Prior experience enhances plasticity in adult visual cortex.
    Nat Neurosci. 2006 Jan;9(1):127-32 PMID: 16327785
  35. A semi-persistent adult ocular dominance plasticity in visual cortex is stabilized by activated CREB.
    Learn Mem. 2004 Nov-Dec;11(6):738-47 PMID: 15537732
  36. Rapid anatomical plasticity of horizontal connections in the developing visual cortex.
    J Neurosci. 2001 May 15;21(10):3476-82 PMID: 11331376
  37. Postnatal development of the visual cortex and the influence of environment.
    Nature. 1982 Oct 14;299(5884):583-91 PMID: 6811951
  38. Molecular basis for induction of ocular dominance plasticity.
    J Neurobiol. 1999 Oct;41(1):83-91 PMID: 10504195
  39. Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex.
    Science. 2000 Mar 17;287(5460):2029-32 PMID: 10720332
  40. Enduring critical period plasticity visualized by transcranial flavoprotein imaging in mouse primary visual cortex.
    J Neurosci. 2006 Nov 8;26(45):11775-85 PMID: 17093098
  41. Critical periods for experience-dependent synaptic scaling in visual cortex.
    Nat Neurosci. 2002 Aug;5(8):783-9 PMID: 12080341
  42. Ephrin-as guide the formation of functional maps in the visual cortex.
    Neuron. 2005 Nov 23;48(4):577-89 PMID: 16301175
  43. Synaptic gain control and homeostasis.
    Curr Opin Neurobiol. 2003 Oct;13(5):560-7 PMID: 14630218
  44. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens.
    J Neurophysiol. 1965 Nov;28(6):1029-40 PMID: 5883730
  45. Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation.
    Nat Neurosci. 2003 Aug;6(8):854-62 PMID: 12886226
  46. Inhibitory threshold for critical-period activation in primary visual cortex.
    Nature. 2000 Mar 9;404(6774):183-6 PMID: 10724170
Article Info
Journal
Neuron
Abbr.
Neuron
ISSN
1097-4199
Published
2008-06-12
Pages
673-80
Language
English
Region
United States
NLM ID
8809320
PMCID
PMC2884387
Subset
IM
Grants
NIMH NIH HHS · P50 MH077972-010003 · United States
NIMH NIH HHS · P50 MH077972 · United States
NEI NIH HHS · R01 EY002874 · United States
NIMH NIH HHS · P50 MH077972-030003 · United States
NIMH NIH HHS · P50 MH077972-020003 · United States
NEI NIH HHS · R01 EY002874-25S1 · United States
NEI NIH HHS · R01 EY002874-26 · United States
Corrections
CommentIn
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]