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The Journal of Neuroscience, April 16, 2008, 28(16):4151-4160; doi:10.1523/JNEUROSCI.4639-07.2008

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Cellular/Molecular
Conical Electron Tomography of a Chemical Synapse: Polyhedral Cages Dock Vesicles to the Active Zone

Guido A. Zampighi,^1,2 Nick Fain,¹ Lorenzo M. Zampighi,³ Francesca Cantele,⁴ Salvatore Lanzavecchia,⁴ and Ernest M. Wright³

¹Department of Neurobiology, ²Jules Stein Eye Research Institute, and ³Department of Physiology, University of California, Los Angeles School of Medicine, Los Angeles, California 90095, and ⁴Department of Structural Chemistry, School of Pharmacy, University of Milan, 20122 Milan, Italy

Correspondence should be addressed to Guido A. Zampighi, Department of Neurobiology, University of California, Los Angeles School of Medicine, Los Angeles, CA 90095. Email: gzampighi{at}mednet.ucla.edu

In this study, we tested the hypothesis that the structure of the active zone of chemical synapses has remained uncertain because of limitations of conventional electron microscopy. To resolve these limitations, we reconstructed chemical synapses of rat neocortex, the archetypical "average" synapse, by conical electron tomography, a method that exhibits an isotropic in plane resolution of 3 nm and eliminates the need to impose symmetry or use averaging methods to increase signal-to-noise ratios. Analysis of 17 reconstructions by semiautomatic density segmentation indicated that the active zone was constructed of a variable number of distinct "synaptic units" comprising a polyhedral cage and a corona of approximately seven vesicles. The polyhedral cages measured 60 nm in diameter, with a density of 44/µm² and were associated with vesicles at the active zone ("first tier"). Vesicles in this first-tier position represented 7.5% of the total number of vesicles in the terminal and were contiguous, hemifused (4% of total), or fully fused (0.5% of total) to the plasma membrane. Our study supports the hypothesis that rat neocortical synapses are constructed of variable numbers of distinct synaptic units that facilitate the docking of vesicles to the active zone and determine the number of vesicles available for immediate release.

Key words: chemical synapses; synaptic vesicles; vesicular pools; docking; hemifusion; cytomatrix

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Received Oct. 11, 2007; revised March 10, 2008; accepted March 11, 2008.

Correspondence should be addressed to Guido A. Zampighi, Department of Neurobiology, University of California, Los Angeles School of Medicine, Los Angeles, CA 90095. Email: gzampighi{at}mednet.ucla.edu

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