Dendritic growth gated by a steroid hormone receptor underlies increases in activity in the developing Drosophila locomotor system

Significance Why do bigger animals have bigger brains, and how do they get them? We find in Drosophila larvae that motoneuron dendrites, the branched structures receiving information from other neurons, grow as the animal gets bigger, and that this is regulated on a cell-by-cell basis by a specific isoform of a steroid hormone receptor, whose functions were unknown. As these dendrites enlarge, they form more connections with presynaptic partners, leading to greater levels of neuronal activity. We propose that these nerve cells increase their activity to compensate for the demands of a bigger body. As animals grow, their nervous systems also increase in size. How growth in the central nervous system is regulated and its functional consequences are incompletely understood. We explored these questions, using the larval Drosophila locomotor system as a model. In the periphery, at neuromuscular junctions, motoneurons are known to enlarge their presynaptic axon terminals in size and strength, thereby compensating for reductions in muscle excitability that are associated with increases in muscle size. Here, we studied how motoneurons change in the central nervous system during periods of animal growth. We find that within the central nervous system motoneurons also enlarge their postsynaptic dendritic arbors, by the net addition of branches, and that these scale with overall animal size. This dendritic growth is gated on a cell-by-cell basis by a specific isoform of the steroid hormone receptor ecdysone receptor-B2, for which functions have thus far remained elusive. The dendritic growth is accompanied by synaptic strengthening and results in increased neuronal activity. Electrical properties of these neurons, however, are independent of ecdysone receptor-B2 regulation. We propose that these structural dendritic changes in the central nervous system, which regulate neuronal activity, constitute an additional part of the adaptive response of the locomotor system to increases in body and muscle size as the animal grows.