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Abstract
Synapse clustering facilitates circuit integration, learning, and memory. Long-term potentiation (LTP) of mature neurons produces synapse enlargement balanced by fewer spines, raising the question of how clusters form despite this homeostatic regulation of total synaptic weight. Three-dimensional reconstruction from serial section electron microscopy (3DEM) revealed the shapes and distributions of smooth endoplasmic reticulum (SER) and polyribosomes, subcellular resources important for synapse enlargement and spine outgrowth. Compared to control stimulation, synapses were enlarged two hours after LTP on resource-rich spines containing polyribosomes (4% larger than control) or SER (15% larger). SER in spines shifted from a single tubule to complex spine apparatus after LTP. Negligible synapse enlargement (0.6%) occurred on resource-poor spines lacking SER and polyribosomes. Dendrites were divided into discrete synaptic clusters surrounded by asynaptic segments. Spine density was lowest in clusters having only resource-poor spines, especially following LTP. In contrast, resource-rich spines preserved neighboring resource-poor spines and formed larger clusters with elevated total synaptic weight following LTP. These clusters also had more shaft SER branches, which could sequester cargo locally to support synapse growth and spinogenesis. Thus, resources appear to be redistributed to synaptic clusters with LTP-related synapse enlargement while homeostatic regulation suppressed spine outgrowth in resource-poor synaptic clusters.
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1 The University of Texas at Austin, Center for Learning and Memory, Department of Neuroscience, Austin, USA (GRID:grid.89336.37) (ISNI:0000 0004 1936 9924); University of Belgrade, Fulbright U.S. Scholar Program, Belgrade, Serbia (GRID:grid.7149.b) (ISNI:0000 0001 2166 9385)
2 The University of Texas at Austin, Center for Learning and Memory, Department of Neuroscience, Austin, USA (GRID:grid.89336.37) (ISNI:0000 0004 1936 9924); McGovern Medical School in Houston, Houston, USA (GRID:grid.89336.37)
3 The University of Texas at Austin, Center for Learning and Memory, Department of Neuroscience, Austin, USA (GRID:grid.89336.37) (ISNI:0000 0004 1936 9924); Google Seattle, Seattle, USA (GRID:grid.89336.37)
4 The University of Texas at Austin, Center for Learning and Memory, Department of Neuroscience, Austin, USA (GRID:grid.89336.37) (ISNI:0000 0004 1936 9924); University of Colorado, Anschutz Medical Campus, Department of Cell and Developmental Biology, Aurora, USA (GRID:grid.430503.1) (ISNI:0000 0001 0703 675X)
5 The University of Texas at Austin, Center for Learning and Memory, Department of Neuroscience, Austin, USA (GRID:grid.89336.37) (ISNI:0000 0004 1936 9924)