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Individual neurons extend multiple processes whose growth cones exhibit different responses to their environment. In culture, detached growth cones display guidance autonomy, contain mRNA for cytoskeletal and other axonal components, and are capable of synthesizing protein locally. However, the extent to which growth cone's autonomy contributes to its pathfinding function within the complex in vivo environment is unknown. Here, we show that detached axonal growth cones from identified Drosophila motoneurons maintain balanced filopodial activities as they extend, navigate and target postsynaptic partner cells normally. After detachment, the growth cones continue to synthesize the synaptic vesicle protein Synaptotagmin but, upon contacting targets, fail to concentrate it at the presynaptic site normally. However, if held by a micropipette that resupplies mechanical tension, the growth cones' ability to localize synaptic vesicles is restored. Our results demonstrate functional autonomy of axonal growth cones as they navigate and initiate synaptogenesis, while implicating intercellular tension as a novel "retrograde" mechanism to adjust synaptic function.


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