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Neuronal morphology underlies circuit connectivity and signal integration, thus profoundly affecting nervous system function. Although microtubules and F-actin have long been recognized as key determinants of dendritic morphology, their precise and distinct roles are yet to be fully elucidated. The lack of arbor-wide cytoskeletal information registered with neuromorphological measurements has so far limited direct observations of the interrelations between microtubules, F-actin and arbor architecture. Here we pair live confocal imaging of fluorescently labeled dendritic arborization (da) neurons in the fruit fly larva with our recently developed multi-signal neural tracing technique. We discovered that dendritic arbor length is highly dependent on local microtubule quantity, whereas local F-actin enrichment is associated with dendritic branching. Earlier computer simulations used quantifiable morphological features both as model parameters (e.g. branch thickness) and emergent properties (e.g. tree asymmetry). Multi-signal reconstructions allowed us to computationally simulate arbor structure solely constrained by experimentally measured, local subcellular distributions of microtubules and F-actin. The generative model yielded synthetic trees with morphological and molecular patterns statistically indistinguishable from those of real da neurons, demonstrating that these two investigated cytoskeletal components are sufficient to define dendritic architecture. The analysis and modeling outcomes hold true for the simplest (Class I) and the most complex (Class IV) da neuron subclasses. Moreover, local increases in the quantity of stable microtubules in Class IV neurons via Formin3 overexpression further strengthens the correlation between local microtubule quantity and dendritic arbor length as predicted by the model and reproduced in simulations. SUPPORT: NIH R01 NS39600 and NS086082 and BICCN U01 MH114829.

Distinct roles of microtubules and actin filaments in defining dendritic architecture