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 Previous Article
The Journal of Neuroscience, May 15, 1999, 19(10):4180-4188
The Incorporation of NMDA Receptors with a Distinct Subunit
Composition at Nascent Hippocampal Synapses In Vitro
Kenneth R.
Tovar and
Gary L.
Westbrook
Vollum Institute, Oregon Health Sciences University, Portland,
Oregon 97201-3098
Activity-dependent synaptic rearrangements during CNS development
require NMDA receptor activation. The control of NMDA receptor function
by developmentally regulated subunit expression has been proposed as
one mechanism for this receptor dependence. We examined the phenotype
of synaptic and extrasynaptic NMDA receptors during the development of
synaptic load using the NMDA receptor 2B (NR2B)-selective antagonist
ifenprodil. In cultured rat hippocampal neurons when relatively few
synapses had formed, the ifenprodil block of EPSCs was less than
whole-cell currents, the latter of which included both synaptic and
extrasynaptic receptors. At the same developmental stage, we found that
extrasynaptic receptors outnumbered synaptic receptors by 3:1; thus
whole-cell currents were dominated by the extrasynaptic population. We
used the macroscopic kinetics of ifenprodil block to distinguish
between the receptor populations. The ifenprodil kinetics of whole-cell
currents from neurons before and during the development of synaptic
load was comparable with that of whole-cell currents in HEK293 cells
transfected with NR1 and NR2B cDNA, indicating that extrasynaptic
receptors are largely NR1/NR2B heteromers. In contrast, synaptic
receptors included both a highly ifenprodil-sensitive (NR1/NR2B)
component as well as a second population with lower ifenprodil
sensitivity; the reduced ifenprodil block of EPSCs was attributable to
synaptic receptors with lower ifenprodil sensitivity rather than to the appearance of ifenprodil-insensitive (NR1/NR2A) receptors. Our data
indicate that the synaptic NMDA receptor complement changes quickly
after synapse formation. We suggest that synapses containing predominately NR1/NR2B heteromers represent "immature" sites, whereas mature sites express NMDA receptors with a distinct, presumably triheteromeric, subunit composition.
Key words:
hippocampus; ifenprodil; NMDA receptors; patch clamp; synapse formation; synaptic load
Copyright © 1999 Society for Neuroscience 0270-6474/99/19104180-09$05.00/0
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K. Nakayama, K. Kiyosue, and T. Taguchi
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M. Mameli, M. Carta, L. D. Partridge, and C. F. Valenzuela
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Y. Aracava, E. F. R. Pereira, A. Maelicke, and E. X. Albuquerque
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K. Erreger, S. M Dravid, T. G Banke, D. J. A Wyllie, and S. F Traynelis
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E. A. Waxman and D. R. Lynch
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Y. N. Dong, E. A. Waxman, and D. R. Lynch
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M. Townsend, Y. Liu, and M. Constantine-Paton
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Y. Lin, V. A. Skeberdis, A. Francesconi, M. V. L. Bennett, and R. S. Zukin
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L. Li, T. H. Murphy, M. R. Hayden, and L. A. Raymond
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S. G. Cull-Candy and D. N. Leszkiewicz
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X.-B. Liu, K. D. Murray, and E. G. Jones
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L. C. Faria and I. Mody
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D. A. Rusakov, A. Scimemi, M. C. Walker, and D. M. Kullmann
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Science,
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T. P. Wong, L. Liu, M. Sheng, and Y. T. Wang
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P. Washbourne, X.-B. Liu, E. G. Jones, and A. K. McAllister
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P. V. Massey, B. E. Johnson, P. R. Moult, Y. P. Auberson, M. W. Brown, E. Molnar, G. L. Collingridge, and Z. I. Bashir
Differential Roles of NR2A and NR2B-Containing NMDA Receptors in Cortical Long-Term Potentiation and Long-Term Depression
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P. E. Bickler
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N. A. Lozovaya, S. E. Grebenyuk, T. Sh. Tsintsadze, B. Feng, D. T. Monaghan, and O. A. Krishtal
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G. Lavezzari, J. McCallum, C. M. Dewey, and K. W. Roche
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L. M. Hawkins, K. Prybylowski, K. Chang, C. Moussan, F. A. Stephenson, and R. J. Wenthold
Export from the Endoplasmic Reticulum of Assembled N-Methyl-D-aspartic Acid Receptors Is Controlled by a Motif in the C Terminus of the NR2 Subunit
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V. M. Andre, J. Flores-Hernandez, C. Cepeda, A. J. Starling, S. Nguyen, M. K. Lobo, H. V. Vinters, M. S. Levine, and G. W. Mathern
NMDA Receptor Alterations in Neurons from Pediatric Cortical Dysplasia Tissue
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A. Scimemi, A. Fine, D. M. Kullmann, and D. A. Rusakov
NR2B-Containing Receptors Mediate Cross Talk among Hippocampal Synapses
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L. Liu, T. P. Wong, M. F. Pozza, K. Lingenhoehl, Y. Wang, M. Sheng, Y. P. Auberson, and Y. T. Wang
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K. Prybylowski and R. J. Wenthold
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K. L. Simpkins, R. P. Guttmann, Y. Dong, Z. Chen, S. Sokol, R. W. Neumar, and D. R. Lynch
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B. Li, Y. Otsu, T. H. Murphy, and L. A. Raymond
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G. Kohr, V. Jensen, H. J. Koester, A. L. A. Mihaljevic, J. K. Utvik, A. Kvello, O. P. Ottersen, P. H. Seeburg, R. Sprengel, and O. Hvalby
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F. Zinebi, J. Xie, J. Liu, R. T. Russell, J. P. Gallagher, M. G. McKernan, and P. Shinnick-Gallagher
NMDA Currents and Receptor Protein Are Downregulated in the Amygdala during Maintenance of Fear Memory
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S. S. Kumar and J. R. Huguenard
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N. O. Dalby and I. Mody
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M. Lopez de Armentia and P. Sah
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Y. Yoshimura, T. Ohmura, and Y. Komatsu
Two Forms of Synaptic Plasticity with Distinct Dependence on Age, Experience, and NMDA Receptor Subtype in Rat Visual Cortex
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S. G. Brickley, C. Misra, M. H. S. Mok, M. Mishina, and S. G. Cull-Candy
NR2B and NR2D Subunits Coassemble in Cerebellar Golgi Cells to Form a Distinct NMDA Receptor Subtype Restricted to Extrasynaptic Sites
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S. Ortinau, B. Laube, and H. Zimmermann
ATP Inhibits NMDA Receptors after Heterologous Expression and in Cultured Hippocampal Neurons and Attenuates NMDA-Mediated Neurotoxicity
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M. Fagiolini, H. Katagiri, H. Miyamoto, H. Mori, S. G. N. Grant, M. Mishina, and T. K. Hensch
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D. E. Chapman, K. A. Keefe, and K. S. Wilcox
Evidence for Functionally Distinct Synaptic NMDA Receptors in Ventromedial Versus Dorsolateral Striatum
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