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Glia and Muscle Sculpt Neuromuscular Arbors by Engulfing Destabilized Synaptic Boutons and Shed Presynaptic Debris

Authors
Journal
PLoS Biology
1544-9173
Publisher
Public Library of Science
Publication Date
Volume
7
Issue
8
Identifiers
DOI: 10.1371/journal.pbio.1000184
Keywords
  • Research Article
  • Neuroscience/Neuronal And Glial Cell Biology
  • Neuroscience/Neuronal Signaling Mechanisms
Disciplines
  • Communication

Abstract

Author Summary The synapse is the fundamental unit of communication between neurons and their target cells. As the nervous system matures, synapses often need to be added, removed, or otherwise remodeled to accommodate the changing needs of the circuit. Such changes are often regulated by the activity of the circuit and are thought to entail the extension or retraction of cellular processes to form or break synaptic connections. We have explored the precise nature of new synapse formation during development of the Drosophila larval neuromuscular junction (NMJ). We find that growing synapses are actually quite wasteful and shed significant amounts of presynaptic membranes and a subset of immature (nonfunctional) synapses. The shedding of this presynaptic material is enhanced by stimulating the activity of the neuron, suggesting that its formation is dependent upon NMJ activity. Surprisingly, we find presynaptic membranes are efficiently removed from the NMJ by two surrounding cell types: glia cells (a neuronal ‘support cell’), which invade the NMJ, and the postsynaptic muscle cell itself. Blocking the ability of these cells to ingest shed presynaptic membranes dramatically reduces new synapse growth, suggesting that the shed presynaptic material is inhibitory to new synapse addition. Therefore, our data demonstrate that actively growing synapses constantly shed membrane material, that glia and muscles work to rapidly clear this from the NMJ, and that the combined efforts of glia and muscles are critical for the proper addition of new synapses to neural circuits.

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