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Science 299 (5612): 1585-1588

Copyright © 2003 by the American Association for the Advancement of Science

Experience Strengthening Transmission by Driving AMPA Receptors into Synapses

Takuya Takahashi,1 Karel Svoboda,2 Roberto Malinow1*

The mechanisms underlying experience-dependent plasticity in the brain may depend on the AMPA subclass of glutamate receptors (AMPA-Rs). We examined the trafficking of AMPA-Rs into synapses in the developing rat barrel cortex. In vivo gene delivery was combined with in vitro recordings to show that experience drives recombinant GluR1, an AMPA-R subunit, into synapses formed between layer 4 and layer 2/3 neurons. Moreover, expression of the GluR1 cytoplasmic tail, a construct that inhibits synaptic delivery of endogenous AMPA-Rs during long-term potentiation, blocked experience-driven synaptic potentiation. In general, synaptic incorporation of AMPA-Rs in vivo conforms to rules identified in vitro and contributes to plasticity driven by natural stimuli in the mammalian brain.

1 Jones Laboratory,
2 Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
*   To whom correspondence should be addressed. E-mail: malinow{at}cshl.org



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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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Y. Qin, Y. Zhu, J. P. Baumgart, R. L. Stornetta, K. Seidenman, V. Mack, L. van Aelst, and J. J. Zhu (2005)
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   Abstract »    Full Text »    PDF »
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P. Steiner, S. Alberi, K. Kulangara, A. Yersin, J.-C. F. Sarria, E. Regulier, S. Kasas, G. Dietler, D. Muller, S. Catsicas, et al. (2005)
EMBO J. 24, 2873-2884
   Abstract »    Full Text »    PDF »
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Q. Li, A. C. Roberts, and D. L. Glanzman (2005)
J. Neurosci. 25, 5623-5637
   Abstract »    Full Text »    PDF »
Postsynaptic Receptor Trafficking Underlying a Form of Associative Learning.
S. Rumpel, J. LeDoux, A. Zador, and R. Malinow (2005)
Science 308, 83-88
   Abstract »    Full Text »    PDF »
Phospholipase D1-Promoted Release of Tissue Plasminogen Activator Facilitates Neurite Outgrowth.
Y. Zhang, Y. Kanaho, M. A. Frohman, and S. E. Tsirka (2005)
J. Neurosci. 25, 1797-1805
   Abstract »    Full Text »    PDF »
Dissociation of experience-dependent and -independent changes in excitatory synaptic transmission during development of barrel cortex.
S. B. Mierau, R. M. Meredith, A. L. Upton, and O. Paulsen (2004)
PNAS 101, 15518-15523
   Abstract »    Full Text »    PDF »
Actin/{alpha}-Actinin-Dependent Transport of AMPA Receptors in Dendritic Spines: Role of the PDZ-LIM Protein RIL.
T. W. Schulz, T. Nakagawa, P. Licznerski, V. Pawlak, A. Kolleker, A. Rozov, J. Kim, T. Dittgen, G. Kohr, M. Sheng, et al. (2004)
J. Neurosci. 24, 8584-8594
   Abstract »    Full Text »    PDF »
Extinction Training Regulates Neuroadaptive Responses to Withdrawal from Chronic Cocaine Self-Administration.
D. W. Self, K.-H. Choi, D. Simmons, J. R. Walker, and C. S. Smagula (2004)
Learn. Mem. 11, 648-657
   Abstract »    Full Text »    PDF »
Alteration of Neuronal Firing Properties after In Vivo Experience in a FosGFP Transgenic Mouse.
A. L. Barth, R. C. Gerkin, and K. L. Dean (2004)
J. Neurosci. 24, 6466-6475
   Abstract »    Full Text »    PDF »
Properties of an Adult Spinal Sensorimotor Circuit Shaped Through Early Postnatal Experience.
P. Petersson, M. Granmo, and J. Schouenborg (2004)
J Neurophysiol 92, 280-288
   Abstract »    Full Text »    PDF »
Experience-dependent Changes in Basal Dendritic Branching of Layer 2/3 Pyramidal Neurons During a Critical Period for Developmental Plasticity in Rat Barrel Cortex.
M. Maravall, I. Y.Y. Koh, W. B. Lindquist, and K. Svoboda (2004)
Cereb Cortex 14, 655-664
   Abstract »    Full Text »    PDF »
How Fast Does the GluR1Qflip Channel Open?.
G. Li and L. Niu (2004)
J. Biol. Chem. 279, 3990-3997
   Abstract »    Full Text »    PDF »
Postsynaptic Density 95 controls AMPA Receptor Incorporation during Long-Term Potentiation and Experience-Driven Synaptic Plasticity.
I. Ehrlich and R. Malinow (2004)
J. Neurosci. 24, 916-927
   Abstract »    Full Text »    PDF »
Development of Columnar Topography in the Excitatory Layer 4 to Layer 2/3 Projection in Rat Barrel Cortex.
K. J. Bender, J. Rangel, and D. E. Feldman (2003)
J. Neurosci. 23, 8759-8770
   Abstract »    Full Text »    PDF »
Maturation of EPSCs and Intrinsic Membrane Properties Enhances Precision at a Cerebellar Synapse.
L. Cathala, S. Brickley, S. Cull-Candy, and M. Farrant (2003)
J. Neurosci. 23, 6074-6085
   Abstract »    Full Text »    PDF »
Ubiquitination, Protein Turnover, and Long-Term Synaptic Plasticity.
J. H. Schwartz (2003)
Sci. STKE 2003, pe26
   Abstract »    Full Text »    PDF »

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