Long-term potentiation (LTP), an increase in synaptic efficacy following high-frequencystimulation, is widely considered a mechanism of learning. LTP involves local remodeling ofdendritic spines and synapses. Smooth endoplasmic reticulum (SER) and endosomal compartmentscould provide local stores of membrane and proteins, bypassing the distant Golgi apparatus. Totest this hypothesis, effects of LTP were compared to control stimulation in rat hippocampal areaCA1 at postnatal day 15 (P15). By two hours, small spines lacking SER increased after LTP, whereaslarge spines did not change in frequency, size, or SER content. Total SER volume decreased afterLTP consistent with transfer of membrane to the added spines. Shaft SER remained more abundantin spiny than aspiny dendritic regions, apparently supporting the added spines. Recyclingendosomes were elevated specifically in small spines after LTP. These findings suggest localsecretory trafficking contributes to LTP-induced synaptogenesis and primes the new spines forfuture plasticity.
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Local resources of polyribosomes and SER promote synapse enlargement and spine clustering after long-term potentiation in adult rat hippocampus
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.
more » « less- Award ID(s):
- 1707356
- NSF-PAR ID:
- 10153496
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 9
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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