Competitive and non-competitive rules govern activity-dependent axon arbor development in vivo

Sensory circuits are assembled early in development. A remarkable feature of this process is that it relies on “spontaneous” electrical activity (SEA) generated within sensory organs. However, our understanding of the way in which SEA affects the assembly of sensory circuits is quite limited. To this end, we used the mechanosensory lateral line in larval zebrafish. Mosaic expression of an exogenous potassium channel was used to suppress electrical activity in single lateralis afferent neurons. Imaging in vivo showed that SEA regulates axon arbor territory and complexity. Moreover, silenced axonal arbors displayed higher motility and lower density of varicosities, both features of immature neurons. We also showed that regulation of arbor territory, branch elimination and formation events are activity-dependent competitive processes, whereas the density of varicosities and branch extension and retraction events are regulated by electrical activity, regardless of activity in neighboring axons. Our study provides in vivo evidence that both competitive and non-competitive rules govern activity-dependent growth and maturation of axon arbors. These findings shed light on the key role that SEA plays in the proper assembly of sensory circuits.