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Rapid Redistribution of Synaptic PSD-95 in the Neocortex In Vivo

Author

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  • Noah W Gray
  • Robby M Weimer
  • Ingrid Bureau
  • Karel Svoboda

Abstract

Most excitatory synapses terminate on dendritic spines. Spines vary in size, and their volumes are proportional to the area of the postsynaptic density (PSD) and synaptic strength. PSD-95 is an abundant multi-domain postsynaptic scaffolding protein that clusters glutamate receptors and organizes the associated signaling complexes. PSD-95 is thought to determine the size and strength of synapses. Although spines and their synapses can persist for months in vivo, PSD-95 and other PSD proteins have shorter half-lives in vitro, on the order of hours. To probe the mechanisms underlying synapse stability, we measured the dynamics of synaptic PSD-95 clusters in vivo. Using two-photon microscopy, we imaged PSD-95 tagged with GFP in layer 2/3 dendrites in the developing (postnatal day 10–21) barrel cortex. A subset of PSD-95 clusters was stable for days. Using two-photon photoactivation of PSD-95 tagged with photoactivatable GFP (paGFP), we measured the time over which PSD-95 molecules were retained in individual spines. Synaptic PSD-95 turned over rapidly (median retention times τr ~ 22–63 min from P10–P21) and exchanged with PSD-95 in neighboring spines by diffusion. PSDs therefore share a dynamic pool of PSD-95. Large PSDs in large spines captured more diffusing PSD-95 and also retained PSD-95 longer than small PSDs. Changes in the sizes of individual PSDs over days were associated with concomitant changes in PSD-95 retention times. Furthermore, retention times increased with developmental age (τr ~ 100 min at postnatal day 70) and decreased dramatically following sensory deprivation. Our data suggest that individual PSDs compete for PSD-95 and that the kinetic interactions between PSD molecules and PSDs are tuned to regulate PSD size. Using two-photon microscopy and photoactivation of a fluorescently tagged synaptic protein (PSD-95), the authors demonstrated rapid turnover of these molecules in dendritic spines of the mouse sensory cortex in vivo.

Suggested Citation

  • Noah W Gray & Robby M Weimer & Ingrid Bureau & Karel Svoboda, 2006. "Rapid Redistribution of Synaptic PSD-95 in the Neocortex In Vivo," PLOS Biology, Public Library of Science, vol. 4(11), pages 1-11, November.
    • Handle: RePEc:plo:pbio00:0040370
    DOI: 10.1371/journal.pbio.0040370
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    References listed on IDEAS

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    2. Lu Chen & Dane M. Chetkovich & Ronald S. Petralia & Neal T. Sweeney & Yoshimi Kawasaki & Robert J. Wenthold & David S. Bredt & Roger A. Nicoll, 2000. "Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms," Nature, Nature, vol. 408(6815), pages 936-943, December.
    3. Jaime Grutzendler & Narayanan Kasthuri & Wen-Biao Gan, 2002. "Long-term dendritic spine stability in the adult cortex," Nature, Nature, vol. 420(6917), pages 812-816, December.
    4. Joshua T. Trachtenberg & Brian E. Chen & Graham W. Knott & Guoping Feng & Joshua R. Sanes & Egbert Welker & Karel Svoboda, 2002. "Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex," Nature, Nature, vol. 420(6917), pages 788-794, December.
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