Mechanical tension contributes to clustering of neurotransmitter vesicles at presynaptic terminals

Memory and learning in animals are mediated by neurotransmitters that are released from vesicles clustered at the synapse. As a synapse is used more frequently, its neurotransmission efficiency increases, partly because of increased vesicle clustering in the presynaptic neuron. Vesicle clustering ha...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2009-08, Vol.106 (31), p.12611-12616
Main Authors: Siechen, Scott, Yang, Shengyuan, Chiba, Akira, Saif, Taher
Format: Article
Language:English
Subjects:
Actins
Actins - physiology
Animal cognition
Animals
Axons
Axons - physiology
Axotomy
Biological Sciences
Cell Adhesion Molecules - physiology
Drosophila
Embryos
Endothelial cells
Insects
Ion Transport
Memory
Neurons
Neurotransmitter Agents - secretion
Neurotransmitters
Physical Sciences
Presynaptic Terminals - physiology
Sensors
Stress, Mechanical
Synapses
Synapses - physiology
Synaptic Vesicles - physiology
Synaptotagmin I - analysis
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Summary:Memory and learning in animals are mediated by neurotransmitters that are released from vesicles clustered at the synapse. As a synapse is used more frequently, its neurotransmission efficiency increases, partly because of increased vesicle clustering in the presynaptic neuron. Vesicle clustering has been believed to result primarily from biochemical signaling processes that require the connectivity of the presynaptic terminal with the cell body, the central nervous system, and the postsynaptic cell. Our in vivo experiments on the embryonic Drosophila nervous system show that vesicle clustering at the neuromuscular presynaptic terminal depends on mechanical tension within the axons. Vesicle clustering vanishes upon severing the axon from the cell body, but is restored when mechanical tension is applied to the severed end of the axon. Clustering increases when intact axons are stretched mechanically by pulling the postsynaptic muscle. Using micro mechanical force sensors, we find that embryonic axons that have formed neuromuscular junctions maintain a rest tension of [almost equal to]1 nanonewton. If the rest tension is perturbed mechanically, axons restore the rest tension either by relaxing or by contracting over a period of [almost equal to]15 min. Our results suggest that neuromuscular synapses employ mechanical tension as a signal to modulate vesicle accumulation and synaptic plasticity.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0901867106